The Microbiome of the Red Sea Coral Stylophora pistillata Is Dominated by Tissue-Associated Endozoicomonas Bacteria

Bayer, Till; Neave, Matthew J.; Alsheikh-­Hussain, Areej; Aranda, Manuel; Yum, Lauren K.; Mincer, Tracy J.; Hughen, Konrad A; Apprill, Amy; Voolstra, Christian R.

doi:10.1128/aem.00695-13

Cited by 249 publications

(266 citation statements)

References 22 publications

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“…Endozoicomonas are Gammaproteobacteria frequently observed in reef‐building corals (Bayer et al., 2013; Bourne et al., 2008; Glasl, Herndl, & Frade, 2016; Neave, Michell, et al., 2017; Neave, Rachmawati, et al., 2017; Pantos, Bongaerts, Dennis, Tyson, & Hoegh‐Guldberg, 2015; Pogoreutz, Rädecker, Cárdenas, Gärdes, Wild, et al., 2017) and highly dominant in pocilloporid hosts where they were found to reside deep within the gastrovascular tissues (Bayer et al., 2013; Neave, Rachmawati, et al., 2017). More generally, Endozoicomonas are commonly assumed to provide an important role in coral holobiont functioning due to their widespread prevalence and high abundance in many coral species (Bayer et al., 2013; Gignoux‐Wolfsohn, Aronson, & Vollmer, 2017; Glasl et al., 2016; Jessen et al., 2013; Meyer, Gunasekera, Scott, Paul, & Teplitski, 2016; Neave et al., 2016; Neave, Rachmawati, et al., 2017) and apparent metabolic versatility (Ding, Shiu, Chen, Chiang, & Tang, 2016; Hyun et al., 2014; Neave, Michell, et al., 2017; Yang et al., 2010).…”

Section: Discussionmentioning

confidence: 99%

“…More generally, Endozoicomonas are commonly assumed to provide an important role in coral holobiont functioning due to their widespread prevalence and high abundance in many coral species (Bayer et al., 2013; Gignoux‐Wolfsohn, Aronson, & Vollmer, 2017; Glasl et al., 2016; Jessen et al., 2013; Meyer, Gunasekera, Scott, Paul, & Teplitski, 2016; Neave et al., 2016; Neave, Rachmawati, et al., 2017) and apparent metabolic versatility (Ding, Shiu, Chen, Chiang, & Tang, 2016; Hyun et al., 2014; Neave, Michell, et al., 2017; Yang et al., 2010). Further, reductions in the abundance of Endozoicomonas in stressed, diseased, or bleached corals are reported in a number of studies, suggesting that pervasive abundance of Endozoicomonas might be an indicator of habitat suitability (Bourne et al., 2008; Cárdenas et al., 2012; Gignoux‐Wolfsohn et al., 2017; Meyer et al., 2016; Morrow et al., 2014; Roder et al., 2015; Röthig et al., 2016; Ziegler et al., 2016).…”

Section: Discussionmentioning

confidence: 99%

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Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

Pogoreutz

Rädecker

Cárdenas

et al. 2018

Ecology and Evolution

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118

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The importance of Symbiodinium algal endosymbionts and a diverse suite of bacteria for coral holobiont health and functioning are widely acknowledged. Yet, we know surprisingly little about microbial community dynamics and the stability of host‐microbe associations under adverse environmental conditions. To gain insight into the stability of coral host‐microbe associations and holobiont structure, we assessed changes in the community structure of Symbiodinium and bacteria associated with the coral Pocillopora verrucosa under excess organic nutrient conditions. Pocillopora‐associated microbial communities were monitored over 14 days in two independent experiments. We assessed the effect of excess dissolved organic nitrogen (DON) and excess dissolved organic carbon (DOC). Exposure to excess nutrients rapidly affected coral health, resulting in two distinct stress phenotypes: coral bleaching under excess DOC and severe tissue sloughing (>90% tissue loss resulting in host mortality) under excess DON. These phenotypes were accompanied by structural changes in the Symbiodinium community. In contrast, the associated bacterial community remained remarkably stable and was dominated by two Endozoicomonas phylotypes, comprising on average 90% of 16S rRNA gene sequences. This dominance of Endozoicomonas even under conditions of coral bleaching and mortality suggests the bacterial community of P. verrucosa may be rather inflexible and thereby unable to respond or acclimatize to rapid changes in the environment, contrary to what was previously observed in other corals. In this light, our results suggest that coral holobionts might occupy structural landscapes ranging from a highly flexible to a rather inflexible composition with consequences for their ability to respond to environmental change.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

Pogoreutz

Rädecker

Cárdenas

et al. 2018

Ecology and Evolution

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118

112

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“…In particular, Endozoicomonas spp. are found to comprise 70 to 95% of the microbiome in several Red Sea (Stylophora pistillata, Pocillopora damicornis, and Acropora humilis) and Caribbean corals (Porites astreoides [49][50][51][52]). These bacteria have also been shown to live endosymbiotically, forming large aggregations deep within coral tissues (51), potentially playing a role in bacterial communication and structuring via the production of quorum-sensing signaling metabolites and antimicrobial compounds (53).…”

Section: Discussionmentioning

confidence: 99%

Allelochemicals Produced by Brown Macroalgae of the Lobophora Genus Are Active against Coral Larvae and Associated Bacteria, Supporting Pathogenic Shifts to Vibrio Dominance

Morrow

Bromhall

Motti

et al. 2017

Appl Environ Microbiol

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Pervasive environmental stressors on coral reefs are attributed with shifting the competitive balance in favor of alternative dominants, such as macroalgae. Previous studies have demonstrated that macroalgae compete with corals via a number of mechanisms, including the production of potent primary and secondary metabolites that can influence coral-associated microbial communities. The present study investigates the effects of the Pacific brown macroalga Lobophora sp. (due to the shifting nature of the Lobophora species complex, it will be referred to here as Lobophora sp.) on coral bacterial isolates, coral larvae, and the microbiome associated with the coral Porites cylindrica. Crude aqueous and organic macroalgal extracts were found to inhibit the growth of coral-associated bacteria. Extracts and fractions were also shown to inhibit coral larval settlement and cause mortality at concentrations lower (Ͻ0.3 mg · ml Ϫ1 ) than calculated natural concentrations (4.4 mg · ml Ϫ1 ). Microbial communities associated with coral tissues exposed to aqueous (e.g., hydrophilic) crude extracts demonstrated a significant shift to Vibrio dominance and a loss of sequences related to the putative coral bacterial symbiont, Endozoicomonas sp., based on 16S rRNA amplicon sequencing. This study contributes to growing evidence that macroalgal allelochemicals, dissolved organic material, and native macroalgal microbial assemblages all play a role in shifting the microbial equilibrium of the coral holobiont away from a beneficial state, contributing to a decline in coral fitness and a shift in ecosystem structure.IMPORTANCE Diverse microbial communities associate with coral tissues and mucus, providing important protective and nutritional services, but once disturbed, the microbial equilibrium may shift from a beneficial state to one that is detrimental or pathogenic. Macroalgae (e.g., seaweeds) can physically and chemically interact with corals, causing abrasion, bleaching, and overall stress. This study contributes to a growing body of evidence suggesting that macroalgae play a critical role in shifting the coral holobiont equilibrium, which may promote the invasion of opportunistic pathogens and cause coral mortality, facilitating additional macroalgal growth and invasion in the reef. Thus, macroalgae not only contribute to a decline in coral fitness but also influence coral reef ecosystem structure.KEYWORDS DNA sequencing, Lobophora, Porites, QIIME, coral larvae, coral reef, holobiont, macroalgae, metagenomics, pathogens

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“…Moreover, coevolution of bacteria and coral has been proposed (Thompson et al, 2015), as it was demonstrated for Endozoicomonas symbionts in corals with contrasting life-history traits and across global scales (Bayer et al, 2013;Neave et al, 2016Neave et al, , 2017. Detailed analysis of these studies revealed fine scale host-Endozoicomonas specific patterns suggesting phylosymbiosis between corals and this bacterial genus.…”

Section: Exaiptasia H2 and Cc7 Strains Only Share A Small Common Micrmentioning

confidence: 99%

Laboratory-Cultured Strains of the Sea Anemone Exaiptasia Reveal Distinct Bacterial Communities

et al. 2017

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Exaiptasia is a laboratory sea anemone model system for stony corals. Two clonal strains are commonly used, referred to as H2 and CC7, that originate from two genetically distinct lineages and that differ in their Symbiodinium specificity. However, little is known about their other microbial associations. Here, we examined and compared the taxonomic composition of the bacterial assemblages of these two symbiotic Exaiptasia strains, both of which have been cultured in the laboratory long-term under identical conditions. We found distinct bacterial microbiota for each strain, indicating the presence of host-specific microbial consortia. Putative differences in the bacterial functional profiles (i.e., enrichment and depletion of various metabolic processes) based on taxonomic inference were also detected, further suggesting functional differences of the microbiomes associated with these lineages. Our study contributes to the current knowledge of the Exaiptasia holobiont by comparing the bacterial diversity of two commonly used strains as models for coral research.

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The Microbiome of the Red Sea Coral Stylophora pistillata Is Dominated by Tissue-Associated Endozoicomonas Bacteria

Cited by 249 publications

References 22 publications

Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

Allelochemicals Produced by Brown Macroalgae of the Lobophora Genus Are Active against Coral Larvae and Associated Bacteria, Supporting Pathogenic Shifts to Vibrio Dominance

Laboratory-Cultured Strains of the Sea Anemone Exaiptasia Reveal Distinct Bacterial Communities

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