Coral Associated Bacteria

The global decline of coral reefs heightens the need to understand how corals respond to changing environmental conditions. Corals are metaorganisms, so-called holobionts, and restructuring of the associated bacterial community has been suggested as a means of holobiont adaptation. However, the potential for restructuring of bacterial communities across coral species in different environments has not been systematically investigated. Here we show that bacterial community structure responds in a coral host-specific manner upon cross-transplantation between reef sites with differing levels of anthropogenic impact. The coral Acropora hemprichii harbors a highly flexible microbiome that differs between each level of anthropogenic impact to which the corals had been transplanted. In contrast, the microbiome of the coral Pocillopora verrucosa remains remarkably stable. Interestingly, upon cross-transplantation to unaffected sites, we find that microbiomes become indistinguishable from bac...

Chemical examination of the octocoral-associated Bacillus species (sp.) DT001 led to the isolation of pumilacidins A (1) and C (2). We investigated the effect of these compounds on the viability of Plasmodium falciparum and the mechanism of pumilacidin-induced death. The use of inhibitors of protein kinase C (PKC) and phosphoinositide 3-kinase (PI3K) was able to prevent the effects of pumilacidins A and C. The results indicated also that pumilacidins inhibit parasite growth via mitochondrial dysfunction and decreased cytosolic Ca2+.

Objectives: Staphylococcus epidermidis is often associated with biofilm infections related to medical implants. The aim of the present study was to find furanones that decrease biofilm formation without irritative or genotoxic effects, or effects on S. epidermidis growth. Methods: After screening including bioluminescence and biofilm assays, 2 furanones out of 11 were chosen for further studies. MIC values of the two furanones were established to determine whether biofilm inhibition effects were ascribed to inhibition of bacterial growth. To further investigate interference with communication, the effect of the furanones was tested in the presence of the autoinducer-2 precursor (S)-4,5-dihydroxy-2,3-pentanedione. The furanones were tested for possible irritative effects by the Hen's egg test chorioallantoic membrane procedure. Finally, potential genotoxic effects in mice were assessed by a membrane array, and effects on global gene expression were investigated by using a microarray representing 30 000 genes of the mouse genome. Results: From the bioluminescence assay, 4 furanones out of 11 were chosen for further biofilm analyses. Biofilm formation by S. epidermidis was significantly decreased by the four furanones tested at concentrations not affecting microbial growth. Two furanones were chosen for further studies: one that decreased biofilm statistically more than the others and one containing two bromo substituents. The two furanones were found to be non-irritative and non-genotoxic at the concentrations used. Conclusions: Furanones may inhibit biofilm formation through interference with quorum sensing and thus represent promising agents for protecting surfaces from being colonized by S. epidermidis.

Bacteria belonging to the genus Pseudovibrio have been frequently found in association with a wide variety of marine eukaryotic invertebrate hosts, indicative of their versatile and symbiotic lifestyle. A recent comparison of the sponge-associated Pseudovibrio genomes has shed light on the mechanisms influencing a successful symbiotic association with sponges. In contrast, the genomic architecture of Pseudovibrio bacteria associated with other marine hosts has received less attention. Here, we performed genus-wide comparative analyses of 18 Pseudovibrio isolated from sponges, coral, tunicates, flatworm, and seawater. The analyses revealed a certain degree of commonality among the majority of sponge- and coral-associated bacteria. Isolates from other marine invertebrate host, tunicates, exhibited a genetic repertoire for cold adaptation and specific metabolic abilities including mucin degradation in the Antarctic tunicate-associated bacterium Pseudovibrio sp. Tun.PHSC04_5.I4. Reducti...

Multidrug-resistant Pseudomonas aeruginosa poses a global challenge due to its virulence and biofilm-forming ability, leading to persistent infections. This study had a dual focus: first, it aimed to investigate the biofilm activity and antibiotic resistance profiles of Pseudomonas aeruginosa isolates obtained from a fish-rearing farm. Second, it explored the potential of algal extracts as effective antibacterial and antibiofilm agents. The study analyzed 23 isolates of P. aeruginosa from the farm, assessing antibiotic resistance and biofilm formation. The antimicrobial and antibiofilm activities of two algal extracts, Arthrospira platensis (cyanobacteria) acetone extract (AAE) and Polysiphonia scopulorum (Rhodophyta) methanol extract (PME), were tested individually and combined (COE). The effects on biofilm-related gene expression were examined. AAE, PME, and COE were evaluated for antimicrobial and antibiofilm properties. Biofilm-related gene expression was measured and the extrac...

Background The coral holobiont is comprised of a highly diverse microbial community that provides key services to corals such as protection against pathogens and nutrient cycling. The coral surface mucus layer (SML) microbiome is very sensitive to external changes and tied to ecosystem functioning, as it constitutes the direct interface between the coral host and the environment. The functional profile of microbial genes in the coral SML is underexplored and the use of shotgun metagenomics is relatively rare among coral microbiome studies. Here we investigate whether the bacterial taxonomic and functional profiles in the coral SML are shaped by the local reef zone and explore their role in coral health and ecosystem functioning. Results The analysis was conducted using metagenomes and metagenome assemble genomes (MAGs) associated with the coral Pseudodiploria strigosa and the water column from two naturally distinct reef environments in Bermuda: inner patch reefs exposed to a fluctu...

Metagenomics is a primary tool for the description of microbial and viral communities. The sheer magnitude of the data generated in each metagenome makes identifying key differences in the function and taxonomy between communities difficult to elucidate. Here we discuss the application of seven different data mining and statistical analyses by comparing and contrasting the metabolic functions of 212 microbial metagenomes within and between 10 environments. Not all approaches are appropriate for all questions, and researchers should decide which approach addresses their questions. This work demonstrated the use of each approach: for example, random forests provided a robust and enlightening description of both the clustering of metagenomes and the metabolic processes that were important in separating microbial communities from different environments. All analyses identified that the presence of phage genes within the microbial community was a predictor of whether the microbial community was host-associated or free-living. Several analyses identified the subtle differences that occur with environments, such as those seen in different regions of the marine environment.

Metagenomics is a primary tool for the description of microbial and viral communities. The sheer magnitude of the data generated in each metagenome makes identifying key differences in the function and taxonomy between communities difficult to elucidate. Here we discuss the application of seven different data mining and statistical analyses by comparing and contrasting the metabolic functions of 212 microbial metagenomes within and between 10 environments. Not all approaches are appropriate for all questions, and researchers should decide which approach addresses their questions. This work demonstrated the use of each approach: for example, random forests provided a robust and enlightening description of both the clustering of metagenomes and the metabolic processes that were important in separating microbial communities from different environments. All analyses identified that the presence of phage genes within the microbial community was a predictor of whether the microbial community was host-associated or free-living. Several analyses identified the subtle differences that occur with environments, such as those seen in different regions of the marine environment.

Local and global stressors have affected coral reef ecosystems worldwide. Switches from coral to algal dominance states and microbialization are the major processes underlying the global decline of coral reefs. However, most of the knowledge concerning microbialization has not considered physical disturbances (e.g., typhoons, waves, and currents). Southern Japan reef systems have developed under extreme physical disturbances. Here, we present analyses of a three-year investigation on the coral reefs of Ishigaki Island that comprised benthic and fish surveys, water quality analyses, metagenomics and microbial abundance data. At the four studied sites, inorganic nutrient concentrations were high and exceeded eutrophication thresholds. The dissolved organic carbon (DOC) concentration (up to 233.3 µM) and microbial abundance (up to 2.5 × 10 5 cell/mL) values were relatively high. The highest vibrio counts coincided with the highest turf cover (∼55-85%) and the lowest coral cover (∼4.4-10.2%) and fish biomass (0.06 individuals/m 2). Microbiome compositions were similar among all sites and were dominated by heterotrophs. Our data suggest that a synergic effect among several regional stressors are driving coral decline. In a high hydrodynamics reef environment, high algal/turf cover, stimulated by eutrophication and low fish abundance due to overfishing, promote microbialization. Together with crownof-thorns starfish (COTS) outbreaks and possible of climate changes impacts, theses coral reefs are likely to collapse.

A key area in marine antifoulant research is the discovery of new environmentally friendly solutions that prevent biofilm formation and associated biocorrosion. Taking into consideration the natural mechanisms of marine organisms to protect against epibiosis, new biomimetic solutions can be utilised against biofouling, and marine bacteria are promising agents. Therefore, the goal of this study was to identify cultivable bacteria with antifouling (AF) activity associated with the sponge Aplysina gerardogreeni. A collection of 63 bacteria was isolated, and the organic extracts were assayed against various microfouler strains (16 bacteria and five microalgae). The results showed that 87% of bacterial extracts were active against the microfoulers tested. Sixteen of them can be considered to possess AF potential and belong to the genera Bacillus, Micrococcus, Paracoccus, Pseudobacter, Pseudovibrio, Psychrobacter, Staphylocuccus and Terribacillus. Bioactivity showed temporal variations; the highest activity was in February and June and the lowest in October. Bacillus bacteria were dominant and showed AF activities throughout the year. The results revealed those marine bacteria sponge-associated and the genus Bacillus in particular, are promising AF agents.

At present our knowledge on the compartmentalization of coral holobiont microbiomes is highly skewed towards the millimetre-thin coral tissue, leaving the diverse coral skeleton microbiome underexplored. Here, we present a genome-centric view of the skeleton of the reef-building corals' Porites lutea and Isopora palifera, through a compendium of ~ 400 high-quality bacterial and archaeal metagenome-assembled genomes (MAGs), spanning 34 phyla and 57 microbial classes. Skeletal microbiomes harboured a diverse array of stress response genes, including dimethylsulfoniopropionate synthesis (dsyB) and metabolism (DMSP lyase). Furthermore, skeletal MAGs encoded an average of 22 ± 15 genes in P. lutea and 28 ± 23 in I. palifera with eukaryotic-like motifs thought to be involved in maintaining host association. We provide comprehensive insights into the putative functional role of the skeletal microbiome on key metabolic processes such as nitrogen fixation, dissimilatory and assimilatory ...

Objectives: Staphylococcus epidermidis is often associated with biofilm infections related to medical implants. The aim of the present study was to find furanones that decrease biofilm formation without irritative or genotoxic effects, or effects on S. epidermidis growth. Methods: After screening including bioluminescence and biofilm assays, 2 furanones out of 11 were chosen for further studies. MIC values of the two furanones were established to determine whether biofilm inhibition effects were ascribed to inhibition of bacterial growth. To further investigate interference with communication, the effect of the furanones was tested in the presence of the autoinducer-2 precursor (S)-4,5-dihydroxy-2,3-pentanedione. The furanones were tested for possible irritative effects by the Hen's egg test chorioallantoic membrane procedure. Finally, potential genotoxic effects in mice were assessed by a membrane array, and effects on global gene expression were investigated by using a microarray representing 30 000 genes of the mouse genome. Results: From the bioluminescence assay, 4 furanones out of 11 were chosen for further biofilm analyses. Biofilm formation by S. epidermidis was significantly decreased by the four furanones tested at concentrations not affecting microbial growth. Two furanones were chosen for further studies: one that decreased biofilm statistically more than the others and one containing two bromo substituents. The two furanones were found to be non-irritative and non-genotoxic at the concentrations used. Conclusions: Furanones may inhibit biofilm formation through interference with quorum sensing and thus represent promising agents for protecting surfaces from being colonized by S. epidermidis.

The cyanobacterial genera Prochlorococcus and Synechococcus are key phototrophic organisms in the open ocean, and ecological interactions between these groups and heterotrophic bacteria have fundamental importance for marine carbon and nutrient cycling. We applied a microfluidic chemotaxis assay to study the chemotactic response of 3 marine bacterial isolates (Pseudoalteromonas haloplanktis, Vibrio alginolyticus and Silicibacter sp. TM1040) to the chemical products of Synechococcus elongatus and Prochlorococcus marinus MED 4Ax. In the ocean, chemical products from these cyanobacteria may be released into the water column via extracellular exudation or cell lysis. Strong and rapid chemotactic responses by all 3 bacterial strains occurred in reaction to the Synechococcus products. P. haloplanktis cells exhibited the strongest attraction, accumulating within the chemoattractant band in concentrations of up to 9-fold above background levels. Positive chemotaxis to Prochlorococcus chemical products also occurred, with P. haloplanktis and Silicibacter sp. TM1040 exhibiting the strongest responses. These observations indicate that marine bacteria can exhibit behavioural responses to the chemical products of Synechococcus and Prochlorococcus, which may support ecological associations between these important populations of marine prokaryotes in the environment.

The global decline of coral reefs heightens the need to understand how corals respond to changing environmental conditions. Corals are metaorganisms, so-called holobionts, and restructuring of the associated bacterial community has been suggested as a means of holobiont adaptation. However, the potential for restructuring of bacterial communities across coral species in different environments has not been systematically investigated. Here we show that bacterial community structure responds in a coral host-specific manner upon cross-transplantation between reef sites with differing levels of anthropogenic impact. The coral Acropora hemprichii harbors a highly flexible microbiome that differs between each level of anthropogenic impact to which the corals had been transplanted. In contrast, the microbiome of the coral Pocillopora verrucosa remains remarkably stable. Interestingly, upon crosstransplantation to unaffected sites, we find that microbiomes become indistinguishable from back-transplanted controls, suggesting the ability of microbiomes to recover. It remains unclear whether differences to associate with bacteria flexibly reflects different holobiont adaptation mechanisms to respond to environmental change.

The skeleton of reef-building coral harbors diverse microbial communities that could compensate for metabolic deficiencies caused by the loss of algal endosymbionts, i.e., coral bleaching. However, it is unknown to what extent endolith taxonomic diversity and functional potential might contribute to thermal resilience. Here we exposed Goniastrea edwardsi and Porites lutea, two common reef-building corals from the central Red Sea to a 17-day long heat stress. Using hyperspectral imaging, marker gene/metagenomic sequencing, and NanoSIMS, we characterized their endolithic microbiomes together with 15 N and 13 C assimilation of two skeletal compartments: the endolithic band directly below the coral tissue and the deep skeleton. The bleaching-resistant G. edwardsi was associated with endolithic microbiomes of greater functional diversity and redundancy that exhibited lower N and C assimilation than endoliths in the bleaching-sensitive P. lutea. We propose that the lower endolithic primary productivity in G. edwardsi can be attributed to the dominance of chemolithotrophs. Lower primary production within the skeleton may prevent unbalanced nutrient fluxes to coral tissues under heat stress, thereby preserving nutrient-limiting conditions characteristic of a stable coral-algal symbiosis. Our findings link coral endolithic microbiome structure and function to bleaching susceptibility, providing new avenues for understanding and eventually mitigating reef loss.

In an attempt to study the antibacterial, antivirulence and antibiofilm potentials of bacteria residing the tissue and surface mucus layers of the pristine corals, we screened a total of 43 distinct bacterial morphotypes from the coral Favites sp. Among the isolates, Pseudomonas aeruginosa strain CBMGL12 with showed antibacterial, antivirulence and antibiofilm activity against multidrug resistant pathogenic strains of Staphylococcus aureus (reference strain: MTCC96; community-acquired methicillin resistant strain: CA-MRSA). Extracellular products (ECP) from the coral-associated bacterium P. aeruginosa were solvent extracted, fractionated by chromatographic techniques such as silica column and HPLC-UV with concomitant bioassays guiding the fractionation of metabolites. Identification of bioactive chemical moieties was performed by FT-IR analysis, GC-MS/MS equipped with NIST library, 1H and 13C NMR spectral studies. We report the differential production of extracellular and cell-assoc...

Natural evolution in microbes exposed to antibiotics causes inevitable selection of resistant mutants. This turns out to be a vicious cycle which requires the continuous discovery of new and effective antibiotics. For the last six decades, we have been relying on semisynthetic derivatives of natural products discovered in "Golden Era" from microbes, especially Streptomyces sp. Low success rates of rational drug-design sparked a resurgence in the invention of novel natural products or scaffolds from untapped or uncommon microbial niches. Therefore, in this study, we examined the microbial diversity inhabiting the yak milk for their ability to produce antimicrobial compounds. We prepared the crude fermentation extracts of fifty isolates from yak milk and screened them against indicator strains for the inhibitory activity. Later, with the aid of gel filtration chromatography followed by reversed-phase HPLC, we isolated one antimicrobial compound Y5-P1 from the strain Y5 (Pseudomonas koreensis) which showed bioactivity against Gram-positive and Gram-negative bacteria. The compound was chemically characterized using HRMS, FTIR, and NMR spectroscopy and identified as 1-acetyl-9H-β-carboline-3-carboxylic acid. It showed minimum inhibitory activity (MIC) in the range of 62.5-250 µg /ml. The cytotoxicity results revealed that IC 50 against two mammalian cell lines i.e., HepG2 and HEK293T was 500 and 750 µg/ml, respectively. This is the first report on the production of this derivative of β-carboline by the microorganism. Also, the study enlightens the importance of microbes residing in uncommon environments or unexplored habitats in the discovery of a diverse array of natural products which could be designed further as drug candidates against highly resistant pathogens.

Original Research Article Skin disease is one of the most common diseases in tropical countries such as Indonesia, which might be caused by infection of pathogens like Staphylococcus aureus and Pseudomonas aeruginosa. Red algae Gracilaria sp. originated from Wediombo Beach, Yogyakarta, Indonesia has not been widely used for medicinal purpose, especially as an antimicrobial for skin diseases in human. Therefore, this research aimed to study about the potency of local Gracilaria sp. extract as an antibacterial against skin disease pathogen. Red algae extraction was carried out using maceration method in ethanol solvent. Identification of phytochemical groups was determined using basic biochemistry analysis and Thin Layer Chromatography (TLC), while active phytochemical compounds were identified using Gas Chromatography-Mass Spectrophotometry (GC-MS). Antibacterial tests were performed by minimum inhibition concentration (MIC) using MTT indicator and inhibition assay using paper disc m...

The global decline of coral reefs heightens the need to understand how corals respond to changing environmental conditions. Corals are metaorganisms, so-called holobionts, and restructuring of the associated bacterial community has been suggested as a means of holobiont adaptation. However, the potential for restructuring of bacterial communities across coral species in different environments has not been systematically investigated. Here we show that bacterial community structure responds in a coral host-specific manner upon cross-transplantation between reef sites with differing levels of anthropogenic impact. The coral Acropora hemprichii harbors a highly flexible microbiome that differs between each level of anthropogenic impact to which the corals had been transplanted. In contrast, the microbiome of the coral Pocillopora verrucosa remains remarkably stable. Interestingly, upon crosstransplantation to unaffected sites, we find that microbiomes become indistinguishable from back-transplanted controls, suggesting the ability of microbiomes to recover. It remains unclear whether differences to associate with bacteria flexibly reflects different holobiont adaptation mechanisms to respond to environmental change.

Metagenomics is a primary tool for the description of microbial and viral communities. The sheer magnitude of the data generated in each metagenome makes identifying key differences in the function and taxonomy between communities difficult to elucidate. Here we discuss the application of seven different data mining and statistical analyses by comparing and contrasting the metabolic functions of 212 microbial metagenomes within and between 10 environments. Not all approaches are appropriate for all questions, and researchers should decide which approach addresses their questions. This work demonstrated the use of each approach: for example, random forests provided a robust and enlightening description of both the clustering of metagenomes and the metabolic processes that were important in separating microbial communities from different environments. All analyses identified that the presence of phage genes within the microbial community was a predictor of whether the microbial community was host-associated or free-living. Several analyses identified the subtle differences that occur with environments, such as those seen in different regions of the marine environment.

An understanding of bacterial diversity and evolution in any environment requires knowledge of phenotypic diversity. In this study, the underlying factors leading to phenotypic clustering were analyzed and interpreted using a novel approach based on a four-tiered graph. Bacterial isolates were organized into equivalence classes based on their phenotypic profile. Likewise, phenotypes were organized in equivalence classes based on the bacteria that manifest them. The linking of these equivalence classes in a four-tiered graph allowed for a quick visual identification of the phenotypic measurements leading to the clustering patterns deduced from principal component analyses. For evaluation of the method, we investigated phenotypic variation in enzyme production and carbon assimilation of members of the genera Pseudomonas and Serratia, isolated from the Aletsch Glacier in Switzerland. The analysis indicates that the genera isolated produce at least six common enzymes and can exploit a wide range of carbon resources, though some specialist species within the pseudomonads were also observed. We further found that pairwise distances between enzyme profiles strongly correlate with distances based on carbon profiles. However, phenotypic distances weakly correlate with phylogenetic distances. The method developed in this study facilitates a more comprehensive understanding of phenotypic clustering than what would be deduced from principal component analysis alone.

Coral reefs are among the most biodiverse biological systems on earth. Corals are classified as marine invertebrates and filter the surrounding food and other particles in seawater, including pathogens such as viruses. Viruses act as both pathogen and symbiont for metazoans. Marine viruses that are abundant in the ocean are mostly single-, double stranded DNA and single-, double stranded RNA viruses. These discoveries were made via advanced identification methods which have detected their presence in coral reef ecosystems including PCR analyses, metagenomic analyses, transcriptomic analyses and electron microscopy. This review discusses the discovery of viruses in the marine environment and their hosts, viral diversity in corals, presence of virus in corallivorous fish communities in reef ecosystems, detection methods, and occurrence of marine viral communities in marine sponges.

Epidermal fish mucus comprises of diverse bioactive metabolites which plays an immense role in defense mechanisms and other important cellular activities. Primarily, this study aims to screen the unexplored mucus extract of Puntius sophore (P. sophore) for its antagonistic potential against common pathogens, which are commonly implicated in foodborne and healthcare associated infections, with effects on their adhesion and biofilm formation. Profiling of the skin mucus was carried out by High Resolution-Liquid Chromatography Mass Spectrometry (HR-LCMS), followed by antibacterial activity and assessment of antibiofilm potency and efficacy on the development, formation, and texture of biofilms. Furthermore, bacterial cell damage, viability within the biofilm, checkerboard test, and cytotoxicity were also evaluated. As a result, P. sophore mucus extract was found to be effective against all tested strains. It also impedes the architecture of biofilm matrix by affecting the viability and...

Corals are animals whose health is often maintained by symbiotic microalgae and other microorganisms, yet they are highly susceptible to environmental-related disturbances. Here, we used a known disruptor, antibiotics, to understand how the coral mucus microbial community reassembles itself following disturbance. ABSTRACT Microbial relationships are critical to coral health, and changes in microbiomes are often exhibited following environmental disturbance. However, the dynamics of coral-microbial composition and external factors that govern coral microbiome assembly and response to disturbance remain largely uncharacterized. Here, we investigated how antibiotic-induced disturbance affects the coral mucus microbiota in the facultatively symbiotic temperate coral Astrangia poculata, which occurs naturally with high (symbiotic) or low (aposymbiotic) densities of the endosymbiotic dinoflagellate Breviolum psygmophilum. We also explored how differences in the mucus microbiome of natural...

Global climate change will have a direct effect on the Great Barrier Reef (GBR) as discussed in previous and subsequent chapters. The primary effect of climate change will be a 1 to 3°C increase in global sea surface temperature along with sea level rises as predicted by Intergovernmental Panel on Climate Change (IPCC) models. Other associated effects include increased acidity and increased terrestrial inputs. The effects of climate change will have a significant impact on marine microbes, potentially altering microbial diversity, function and community dynamics. Although microbes constitute by far the largest diversity and biomass of all marine organisms, they are often ignored in discussions about the impacts of climate change (Figure 5.1). This is despite the fact that the vast microbial life on our planet plays a central role in either accentuating or mitigating the effects of climate change. Since microbes are central to the global cycles (including carbon, nitrogen and trace gases), changes to temperature, nutrient availability and environmental pH will have major impacts on microbial processes central to the climate debate. This chapter will discuss the exposure, sensitivity and impacts of climate change on marine microbes at global, regional and local scales, providing examples of observed impacts in marine ecosystems. In doing so, the adaptive capacity and vulnerability of marine microbes to climate change will be assessed. The background provided in this chapter emphasises the importance of marine microbes and outlines why they require greater appreciation in research effort and consideration in predictive climate models. 5.1.1 Tropical marine microbes With more than a billion microorganisms in a litre of sea water, the biodiversity of microbial communities (Figure 5.1) and the functional roles they play in the marine environment (Figures 5.2 and 5.3) are hugely significant. Limitations with traditional culture-based methodologies (generally only 0.1% to 1% of marine microbes can be recovered on culture media by conventional approaches) mean that the diversity, phylogeny and function of marine microbes have remained largely unexplored. However, with the advent of molecular techniques, we are now discovering a huge diversity of marine microorganisms 90 and uncovering a wide range of previously unknown microbial functions 35,52,43. The functions and species composition of bacterial communities across the globe, including those of the GBR, may be adversely or positively affected by climate change. Shifts in microbial community structure may subsequently enhance or mitigate the effects of further climate change. Marine microbes are highly abundant, with global oceanic densities estimated at 3.6 x 10 29 bacterial cells 90 , 1.3 x 10 28 archaeal cells 58 and 4 x 10 30 viruses 92. Currently, estimates of marine bacterial diversity range from only a few thousand species 42 to as many as two million distinct taxa 19. Most analyses use a criterion of more than 97 percent sequence identity in the small subunit of ribosomal RNA to define a species or taxon. However, Fuhrman 33 points out that physiological and genomic differences may indicate a division on an even finer scale, suggesting that previous estimates of marine bacterial diversity may be too low 33. Additionally, recent research by Sogin et al. 90 examined microbial diversity in the North Atlantic and discovered that, while a relatively small number of microbes dominate, thousands of low-abundance microbes actually account for the majority of phylogenetic diversity. Sogin et al. 90 concluded that 'this rare biosphere is very ancient and may represent a nearly inexhaustible source of genomic innovation'. Part II: Species and species groups 99 Climate Change and the Great Barrier Reef: A Vulnerability Assessment Chapter 5: Vulnerability of marine microbes on the Great Barrier Reef to climate change Climate Change and the Great Barrier Reef: A Vulnerability Assessment Part II: Species and species groups Figure 5.3 An overview of the classical food chain and microbial loop (Adapted from DeLong and Karl 24) 5.1.2 The functional role of marine microbes 5.1.2.1 Nutrient cycling Changes in rates of bacterial photosynthesis or inorganic flux through the microbial loop can have major impacts on carbon cycling and on global climate. Bacteria are estimated to be responsible for 20 to 50 percent of marine primary productivity 16,29 and perform fundamental roles in the degradation of organic matter. In the upper 500 metres of the ocean, microbes consume an estimated 75 percent of the sinking particulate organic carbon flux 16. Marine microbes are also crucial to various bio-geochemical processes such as nitrogen fixation, chemolithoautotrophy, sulfate reduction and fermentation. Environmental perturbations that affect bacterial abundance or community composition are therefore likely to have large-scale effects on ecosystem function. The traditional view of the marine carbon cycle was that eukaryotic organisms were the only important players in the transfer of carbon between trophic levels. Bacterial processes were largely ignored because bacteria were thought to be inactive and present in low numbers. It is now clear that this historical view of carbon flux from photosynthetic phytoplankton to herbivorous zooplankton to higher organisms is incomplete and the microbial loop needs to be considered in addition to this grazing food chain (Figure 5.3). This paradigm shift has come about over the past 30 years as Classic food chain Microbial food web CO2 Carbon flux

It has been proposed that the chemical composition of a coral's mucus can influence the associated bacterial community. However, information on this topic is rare, and nonexistent for corals that are under thermal stress. This study therefore compared the carbohydrate composition of mucus in the coral Acropora muricata when subjected to increasing thermal stress from 26 to 31 • C, and determined whether this composition correlated with any changes in the bacterial community. Results showed that, at lower temperatures, the main components of mucus were N-acetyl glucosamine and C6 sugars, but these constituted a significantly lower proportion of the mucus in thermally stressed corals. The change in the mucus composition coincided with a shift from a γ-Proteobacteria-to a Verrucomicrobiae-and α-Proteobacteria-dominated community in the coral mucus. Bacteria in the class Cyanobacteria also started to become prominent in the mucus when the coral was thermally stressed. The increase in the relative abundance of the Verrucomicrobiae at higher temperature was strongly associated with a change in the proportion of fucose, glucose, and mannose in the mucus. Increase in the relative abundance of α-Proteobacteria were associated with GalNAc and glucose, while the drop in relative abundance of γ-Proteobacteria at high temperature coincided with changes in fucose and mannose. Cyanobacteria were highly associated with arabinose and xylose. Changes in mucus composition and the bacterial community in the mucus layer occurred at 29 • C, which were prior to visual signs of coral bleaching at 31 • C. A compositional change in the coral mucus, induced by thermal stress could therefore be a key factor leading to a shift in the associated bacterial community. This, in turn, has the potential to impact the physiological function of the coral holobiont.

Epidermal fish mucus comprises of diverse bioactive metabolites which plays an immense role in defense mechanisms and other important cellular activities. Primarily, this study aims to screen the unexplored mucus extract of Puntius sophore (P. sophore) for its antagonistic potential against common pathogens, which are commonly implicated in foodborne and healthcare associated infections, with effects on their adhesion and biofilm formation. Profiling of the skin mucus was carried out by High Resolution-Liquid Chromatography Mass Spectrometry (HR-LCMS), followed by antibacterial activity and assessment of antibiofilm potency and efficacy on the development, formation, and texture of biofilms. Furthermore, bacterial cell damage, viability within the biofilm, checkerboard test, and cytotoxicity were also evaluated. As a result, P. sophore mucus extract was found to be effective against all tested strains. It also impedes the architecture of biofilm matrix by affecting the viability and...

Pseudoalteromonas sp. strain OCN003 is a marine gammaproteobacterium that was isolated from a diseased colony of the common Hawaiian reef coral, Montipora capitata, found on a reef surrounding Moku o Lo'e in Ka ne'ohe Bay, Hawaii. Here, we report the complete genome of Pseudoalteromonas sp. strain OCN003.

Background Microbiome manipulation could enhance heat tolerance and help corals survive the pressures of ocean warming. We conducted coral microbiome transplantation (CMT) experiments using the reef-building corals, Pocillopora and Porites, and investigated whether this technique can benefit coral heat resistance while modifying the bacterial microbiome. Initially, heat-tolerant donors were identified in the wild. We then used fresh homogenates made from coral donor tissues to inoculate conspecific, heat-susceptible recipients and documented their bleaching responses and microbiomes by 16S rRNA gene metabarcoding. Results Recipients of both coral species bleached at lower rates compared to the control group when exposed to short-term heat stress (34 °C). One hundred twelve (Pocillopora sp.) and sixteen (Porites sp.) donor-specific bacterial species were identified in the microbiomes of recipients indicating transmission of bacteria. The amplicon sequence variants of the majority of ...

The cyanobacterial genera Prochlorococcus and Synechococcus are key phototrophic organisms in the open ocean, and ecological interactions between these groups and heterotrophic bacteria have fundamental importance for marine carbon and nutrient cycling. We applied a microfluidic chemotaxis assay to study the chemotactic response of 3 marine bacterial isolates (Pseudoalteromonas haloplanktis, Vibrio alginolyticus and Silicibacter sp. TM1040) to the chemical products of Synechococcus elongatus and Prochlorococcus marinus MED 4Ax. In the ocean, chemical products from these cyanobacteria may be released into the water column via extracellular exudation or cell lysis. Strong and rapid chemotactic responses by all 3 bacterial strains occurred in reaction to the Synechococcus products. P. haloplanktis cells exhibited the strongest attraction, accumulating within the chemoattractant band in concentrations of up to 9-fold above background levels. Positive chemotaxis to Prochlorococcus chemical products also occurred, with P. haloplanktis and Silicibacter sp. TM1040 exhibiting the strongest responses. These observations indicate that marine bacteria can exhibit behavioural responses to the chemical products of Synechococcus and Prochlorococcus, which may support ecological associations between these important populations of marine prokaryotes in the environment.

Sea anemones produce many biologically active compounds including neurotoxins, pore-forming toxins, phospholipases and proteinase inhibitors. The Persian Gulf is an unexplored environment and maybe a rich source of marine natural products. The aim of this study is screening and identification of bioactive metabolites from Stichodactyla haddoni (Haddon's sea anemone) collected at the Persian Gulf. The crude extract of the sea anemone (tentacle, disc and total body) was obtained by methanol solvent. The antibacterial assays were carried out by the disc diffusion method. The antibiofilm activity (biofilm formation, biofilm destruction and reduction of metabolic activity) of the sea anemone extracts was evaluated by microtiter plate method. The bioactive compounds were identified by GC-MS analysis. Data showed that the best antibacterial effect (relate to P. aeruginosa) is obtained from extracts of ''total body'' section. Values of minimum inhibitory concentration and minimum bactericidal concentration show that the maximum antibacterial activity takes place at 10-20 mg/ml concentration. Three parts of sea anemone exhibit different inhibition against biofilm of bacteria, in particular, inhibition of biofilm observed by the tentacle, disc and total body against P. aeruginosa, K. pneumonia and A. baumannii, respectively. Biofilm of P. aeruginosa was the most sensitive and the biofilm of B. cereus was the most resistant structure between all pathogenic bacteria. The best reduction in the metabolic activity was observed in P. aeruginosa and K. pneumonia among tested bacteria. Aliphatic compounds were predominant bioactive metabolites in this sea anemone. The marine animal and especially sea anemone produce useful bioactive compounds that can be used to prevent bacterial biofilm; application of bioactive materials, reported in this study, can be proposed for future studies.

Global climate change will have a direct effect on the Great Barrier Reef (GBR) as discussed in previous and subsequent chapters. The primary effect of climate change will be a 1 to 3°C increase in global sea surface temperature along with sea level rises as predicted by Intergovernmental Panel on Climate Change (IPCC) models. Other associated effects include increased acidity and increased terrestrial inputs. The effects of climate change will have a significant impact on marine microbes, potentially altering microbial diversity, function and community dynamics. Although microbes constitute by far the largest diversity and biomass of all marine organisms, they are often ignored in discussions about the impacts of climate change (Figure 5.1). This is despite the fact that the vast microbial life on our planet plays a central role in either accentuating or mitigating the effects of climate change. Since microbes are central to the global cycles (including carbon, nitrogen and trace gases), changes to temperature, nutrient availability and environmental pH will have major impacts on microbial processes central to the climate debate. This chapter will discuss the exposure, sensitivity and impacts of climate change on marine microbes at global, regional and local scales, providing examples of observed impacts in marine ecosystems. In doing so, the adaptive capacity and vulnerability of marine microbes to climate change will be assessed. The background provided in this chapter emphasises the importance of marine microbes and outlines why they require greater appreciation in research effort and consideration in predictive climate models. 5.1.1 Tropical marine microbes With more than a billion microorganisms in a litre of sea water, the biodiversity of microbial communities (Figure 5.1) and the functional roles they play in the marine environment (Figures 5.2 and 5.3) are hugely significant. Limitations with traditional culture-based methodologies (generally only 0.1% to 1% of marine microbes can be recovered on culture media by conventional approaches) mean that the diversity, phylogeny and function of marine microbes have remained largely unexplored. However, with the advent of molecular techniques, we are now discovering a huge diversity of marine microorganisms 90 and uncovering a wide range of previously unknown microbial functions 35,52,43. The functions and species composition of bacterial communities across the globe, including those of the GBR, may be adversely or positively affected by climate change. Shifts in microbial community structure may subsequently enhance or mitigate the effects of further climate change. Marine microbes are highly abundant, with global oceanic densities estimated at 3.6 x 10 29 bacterial cells 90 , 1.3 x 10 28 archaeal cells 58 and 4 x 10 30 viruses 92. Currently, estimates of marine bacterial diversity range from only a few thousand species 42 to as many as two million distinct taxa 19. Most analyses use a criterion of more than 97 percent sequence identity in the small subunit of ribosomal RNA to define a species or taxon. However, Fuhrman 33 points out that physiological and genomic differences may indicate a division on an even finer scale, suggesting that previous estimates of marine bacterial diversity may be too low 33. Additionally, recent research by Sogin et al. 90 examined microbial diversity in the North Atlantic and discovered that, while a relatively small number of microbes dominate, thousands of low-abundance microbes actually account for the majority of phylogenetic diversity. Sogin et al. 90 concluded that 'this rare biosphere is very ancient and may represent a nearly inexhaustible source of genomic innovation'. Part II: Species and species groups 99 Climate Change and the Great Barrier Reef: A Vulnerability Assessment Chapter 5: Vulnerability of marine microbes on the Great Barrier Reef to climate change Climate Change and the Great Barrier Reef: A Vulnerability Assessment Part II: Species and species groups Figure 5.3 An overview of the classical food chain and microbial loop (Adapted from DeLong and Karl 24) 5.1.2 The functional role of marine microbes 5.1.2.1 Nutrient cycling Changes in rates of bacterial photosynthesis or inorganic flux through the microbial loop can have major impacts on carbon cycling and on global climate. Bacteria are estimated to be responsible for 20 to 50 percent of marine primary productivity 16,29 and perform fundamental roles in the degradation of organic matter. In the upper 500 metres of the ocean, microbes consume an estimated 75 percent of the sinking particulate organic carbon flux 16. Marine microbes are also crucial to various bio-geochemical processes such as nitrogen fixation, chemolithoautotrophy, sulfate reduction and fermentation. Environmental perturbations that affect bacterial abundance or community composition are therefore likely to have large-scale effects on ecosystem function. The traditional view of the marine carbon cycle was that eukaryotic organisms were the only important players in the transfer of carbon between trophic levels. Bacterial processes were largely ignored because bacteria were thought to be inactive and present in low numbers. It is now clear that this historical view of carbon flux from photosynthetic phytoplankton to herbivorous zooplankton to higher organisms is incomplete and the microbial loop needs to be considered in addition to this grazing food chain (Figure 5.3). This paradigm shift has come about over the past 30 years as Classic food chain Microbial food web CO2 Carbon flux

In an attempt to study the antibacterial, antivirulence and antibiofilm potentials of bacteria residing the tissue and surface mucus layers of the pristine corals, we screened a total of 43 distinct bacterial morphotypes from the coral Favites sp. Among the isolates, Pseudomonas aeruginosa strain CBMGL12 with showed antibacterial, antivirulence and antibiofilm activity against multidrug resistant pathogenic strains of Staphylococcus aureus (reference strain: MTCC96; community-acquired methicillin resistant strain: CA-MRSA). Extracellular products (ECP) from the coral-associated bacterium P. aeruginosa were solvent extracted, fractionated by chromatographic techniques such as silica column and HPLC-UV with concomitant bioassays guiding the fractionation of metabolites. Identification of bioactive chemical moieties was performed by FT-IR analysis, GC-MS/MS equipped with NIST library, 1 H and 13 C NMR spectral studies. We report the differential production of extracellular and cell-associated virulence and biofilm phenotypes in multi-drug resistant strains of S. aureus, posttreatment with the ECP containing aromatic fatty acid methyl esters (FAME) such as methyl benzoate and methyl phenyl acetate produced by a coral-associated bacterium. In conclusion, this study has identified antibacterial, antibiofilm and antivirulent FAME from the coral-associated P. aeruginosa for its ability to attenuate virulence and biofilms phenotypes in multi-drug resistant pathogenic strains of S. aureus.

Over the past 30 years, the stony coral Acropora palmata has experienced an excessive loss of individuals showing few signs of recovery throughout the Mexican Caribbean, resulting in long stretches of coral rubble structures. When the coral dies, the skeleton begins to be colonized by algae, sponges, virus, bacteria and other microorganisms, forming a new community. Here we analyze, using a metagenomic approach, the diversity and biogeochemical cycles associated to coral rubble in La Bocana (Puerto Morelos, QRoo, Mexico). This study provides the first broad characterization of coral rubble associated communities and their role in biogeochemical cycling, suggesting a potential view of a world where coral reefs are no longer dominated by corals.

Sponge diversity has been reported to decrease from well-preserved to polluted environments, but whether diversity and intra-species variation of their associated microbiomes also change as function of environmental quality remains unknown. Our study aimed to assess whether microbiome composition and structure are related to the proliferation of some sponges and not others under degraded conditions. We characterized the most frequent sponges and their associated bacteria in two close areas (impacted and well-preserved) of Nha Trang Bay (Indo-Pacific). Sponge assemblages were richer and more diverse in the well-preserved reefs, but more abundant (individuals/m. transect) in the impacted environments, where two species (Clathria reinwardti and Amphimedon paraviridis) dominated. Sponge microbiomes from the polluted zones had, in general, lower bacterial diversity and core size and consequently, higher intra-species dispersion than microbiomes of sponges from the well-preserved environments. Microbial communities reflect the reduction of diversity and richness shown by their host sponges. In this sense, sponges with less complex and more variable microbiomes proliferate under degraded environmental conditions, following the ecological paradigm that negatively correlates community diversity and environmental degradation. Thereby, the diversity and structure of sponge microbiomes might indirectly determine the presence and proliferation of sponge species in certain habitats.

Corals exude large volumes of nutrient-containing mucus when exposed to air during low spring tides, as a protective mechanism against desiccation and UV radiation. Currents and waves of the incoming flood detach the mucus from the corals, thereby increasing organic carbon and nutrient concentrations in the reef water. During transport into the reef lagoon, a large fraction of the mucus dissolves. Roller-table experiments demonstrated that this dissolved mucus leads to the formation of marine snow. The non-dissolving gel-like fraction of the mucus rapidly accumulates suspended particles from the flood water and forms in temporal sequence mucus strings, flocs, surface films, surface layers and thick mucus floats. In a platform reef in the Great Barrier Reef, Australia, we characterized each of these mucus phases and observed the exponential increase of algal and bacterial cells in the ageing mucus aggregates. Within 3 hours, the dry weight of the aggregates increased 35-fold, chlorophyll a 192-fold, bacteria cell density 546-fold, C 26-fold, and N 79-fold. After waves destroy the buoyant mucus floats, the mucus aggregates release enclosed gas bubbles and quickly sink to the lagoon sediments, where they are consumed by the benthic community. This releases aggregate-bound nutrients, which fuel benthic and planktonic production in the lagoon. During ebb tide, corals filter the lagoon water and close the recycling loop. We conclude that coral mucus enhances the filtration capacity of coral reefs and fuels reef benthos, thereby increasing the import of oceanic particles and enhancing recycling in the reef ecosystem.

Background: Endolithic microbes in coral skeletons are known to be a nutrient source for the coral host. In addition to aerobic endolithic algae and Cyanobacteria, which are usually described in the various corals and form a green layer beneath coral tissues, the anaerobic photoautotrophic green sulfur bacteria (GSB) Prosthecochloris is dominant in the skeleton of Isopora palifera. However, due to inherent challenges in studying anaerobic microbes in coral skeleton, the reason for its niche preference and function are largely unknown. Results: This study characterized a diverse and dynamic community of endolithic microbes shaped by the availability of light and oxygen. In addition, anaerobic bacteria isolated from the coral skeleton were cultured for the first time to experimentally clarify the role of these GSB. This characterization includes GSB's abundance, genetic and genomic profiles, organelle structure, and specific metabolic functions and activity. Our results explain the advantages endolithic GSB receive from living in coral skeletons, the potential metabolic role of a clade of coralassociated Prosthecochloris (CAP) in the skeleton, and the nitrogen fixation ability of CAP. Conclusion: We suggest that the endolithic microbial community in coral skeletons is diverse and dynamic and that light and oxygen are two crucial factors for shaping it. This study is the first to demonstrate the ability of nitrogen uptake by specific coral-associated endolithic bacteria and shed light on the role of endolithic bacteria in coral skeletons.

Over the last decade, significant advances have been made in characterization of the coral microbiota. Shifts in its composition often correlate with the appearance of signs of diseases and/or bleaching, thus suggesting a link between microbes, coral health and stability of reef ecosystems. The understanding of interactions in coral-associated microbiota is informed by the on-going characterization of other microbiomes, which suggest that metabolic pathways and functional capabilities define the ‘core’ microbiota more accurately than the taxonomic diversity of its members. Consistent with this hypothesis, there does not appear to be a consensus on the specificity in the interactions of corals with microbial commensals, even though recent studies report potentially beneficial functions of the coral-associated bacteria. They cycle sulphur, fix nitrogen, produce antimicrobial compounds, inhibit cell-to-cell signalling and disrupt virulence in opportunistic pathogens. While their benefi...

Global change is altering oceanic temperature, salinity, pH, and oxygen concentration, directly and indirectly influencing marine microbial food web structure and function. As microbes represent >90% of the ocean’s biomass and are major drivers of biogeochemical cycles, understanding their responses to such changes is fundamental for predicting the consequences of global change on ecosystem functioning. Recent findings indicate that marine archaea and archaeal viruses are active and relevant components of marine microbial assemblages, far more abundant and diverse than was previously thought. Further research is urgently needed to better understand the impacts of global change on virus–archaea dynamics and how archaea and their viruses can interactively influence the ocean’s feedbacks on global change.

As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbi...

Konzo, a distinct upper motor neuron disease associated with a cyanogenic diet and chronic malnutrition, predominately affects children and women of childbearing age in sub-Saharan Africa. While the exact biological mechanisms that cause this disease have largely remained elusive, host-genetics and environmental components such as the gut microbiome have been implicated. Using a large study population of 180 individuals from the Democratic Republic of the Congo, where konzo is most frequent, we investigate how the structure of the gut microbiome varied across geographical contexts, as well as provide the first insight into the gut flora of children affected with this debilitating disease using shotgun metagenomic sequencing. Our findings indicate that the gut microbiome structure is highly variable depending on region of sampling, but most interestingly, we identify unique enrichments of bacterial species and functional pathways that potentially modulate the susceptibility of konzo ...

Enzymes have replaced or decreased usage of toxic chemicals for industrial and medical applications leading toward sustainable chemistry. In this study, we report purification and characterization of a biofilm degrading protease secreted by Microbacterium sp. SKS10. The protease was identified as a metalloprotease, Peptidase M16 using mass spectrometry. It showed optimum activity at 60 • C, pH 12 and retained its activity in the presence of various salts and organic solvents. The enzyme was able to degrade biofilms efficiently at enzyme concentration lower than other known enzymes such as papain, trypsin and α-amylase. The presence of this protease increased the accessibility of antibiotics inside the biofilm, and was found to be non-cytotoxic toward human epidermoid carcinoma cells (A431) at the effective concentration for biofilm degradation. Thus, this protease may serve as an effective tool for management of biofilms.

Tropical coral reefs harbour a reservoir of enormous biodiversity that is increasingly threatened by direct human activities and indirect global climate shifts. Emerging coral diseases are one serious threat implicated in extensive reef deterioration through disruption of the integrity of the coral holobionta complex symbiosis between the coral animal, endobiotic alga and an array of microorganisms. In this article, we review our current understanding of the role of microorganisms in coral health and disease, and highlight the pressing interdisciplinary research priorities required to elucidate the mechanisms of disease. We advocate an approach that applies knowledge gained from experiences in human and veterinary medicine, integrated into multidisciplinary studies that investigate the interactions between host, agent and environment of a given coral disease. These approaches include robust and precise disease diagnosis, standardised ecological methods and application of rapidly developing DNA, RNA and protein technologies, alongside established histological, microbial ecology and ecological expertise. Such approaches will allow a better understanding of the causes of coral mortality and coral reef declines and help assess potential management options to mitigate their effects in the longer term.

LLR. During HHR C:H << 0.05 and Gammaproteobacteria approximated 50% of the most abundant organisms in seawater. Alteromonadales, Oceanospirillales, and Thaumarchaeota were the dominant bacteria and archaea. Prevailing metabolisms were related to membrane transport, virulence, disease, and defense. Phages targeting heterotrophs and virulence factor genes characterized HHR. Shifts were also observed in coral microbiomes, according to both annotation-indepent and-dependent methods. HHR bleached corals metagenomes were the most dissimilar and could be distinguished by their di-and tetranucleotides frequencies, Iron Acquision metabolism and virulence genes, such as V. cholerae-related virulence factors. The healthy coral holobiont was shown to be less sensitive to transient seawater-related perturbations than the diseased animals. A conceptual model for the turbulence-induced shifts is put forward.

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Black Band Disease (BBD), the destructive microbial consortium dominated by the cyanobacterium Roseofilum reptotaenium, affects corals worldwide. While the taxonomic composition of BBD consortia has been well-characterized, substantially less is known about its functional repertoire. We sequenced the metagenomes of Caribbean and Pacific black band mats and cultured Roseofilum and obtained five metagenome-assembled genomes (MAGs) of Roseofilum, nine of Proteobacteria, and 12 of Bacteroidetes. Genomic content analysis suggests that Roseofilum is a source of organic carbon and nitrogen, as well as natural products that may influence interactions between microbes. Proteobacteria and Bacteroidetes members of the disease consortium are suited to the degradation of amino acids, proteins, and carbohydrates. The accumulation of sulfide underneath the black band mat, in part due to a lack of sulfur oxidizers, contributes to the lethality of the disease. The presence of sulfide:quinone oxidore...