Distinguishing between Microbial Habitats Unravels Ecological Complexity in Coral Microbiomes

Apprill, Amy; Weber, Laura; Santoro, Alyson E.

doi:10.1128/msystems.00143-16

Cited by 99 publications

(93 citation statements)

References 71 publications

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“…Several of these taxa have been commonly associated with corals and coral‐derived organic matter (OM) (Nelson et al ), and Gammaproteobacteria are typically early colonizers of marine surfaces (Dang and Lovell ; Sweet et al ). Endozoicomonas are an established tissue and mucus symbiont of corals globally (Apprill et al ; Glasl et al ; Neave et al ; Pollock et al ), and our results extend the current knowledge of Endozoicomonas biogeography by indicating that Endozoicomonas may reside in the seawater surrounding corals (specifically P. astreoides ). The other enriched bacteria, including members within the genus Bermanella and the order Alteromonadales , have previously been found in association with coral‐derived particulate and dissolved OM including coral tissue homogenates (Randall et al ), coral mucus (Sweet et al ), the seawater close to corals (Tout et al ), and within natural RSW cultures inoculated with coral mucus and exudates (Allers et al ; Nelson et al ).…”

Section: Discussionsupporting

confidence: 83%

“…Future studies could investigate the connection between water flow and microbial dynamics within coral ecospheres. The variability in microbial community similarity between RSW samples collected within JR also corroborates the strong influence of reef‐specific environmental conditions but is within the range of variability observed in seawater microbial communities at smaller geographic scales (Apprill et al ). Future studies of the dynamic environment of the coral ecosphere should undoubtedly account for reef‐specific variation by collecting more ecosphere samples (biological replicates) at each site for every species surveyed.…”

Section: Discussionsupporting

confidence: 70%

“…While collecting paired RSW and CSW samples would have been ideal, we had limited bottom time to collect paired samples using our syringe sampling approach. Instead, we opted to integrate the RSW samples per reef based on previous observations of relatively high similarity in RSW microbial communities across individual reefs (Apprill et al ). To collect RSW samples, seawater was pumped to the surface from reef depth (> 1 m off of the reef substrate) with a groundwater pump (Mini‐monsoon sampling pump, Proactive Environmental Products).…”

Section: Methodsmentioning

confidence: 99%

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The coral ecosphere: A unique coral reef habitat that fosters coral–microbial interactions

Weber

González‐Díaz

Armenteros

et al. 2019

Limnology & Oceanography

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Scleractinian corals are bathed in a sea of planktonic and particle‐associated microorganisms. The metabolic products of corals influence the growth and composition of microorganisms, but interactions between corals and seawater microorganisms are underexplored. We conducted a field‐based survey to compare the biomass, diversity, composition, and functional capacity of microorganisms in small‐volume seawater samples collected adjacent to five coral species with seawater collected > 1 m away from the reef substrate on the same reefs. Seawater collected close to corals generally harbored copiotrophic‐type bacteria and its bacterial and archaeal composition was influenced by coral species as well as the local reef environment. Trends in picoplankton abundances were variable and either increased or decreased away from coral colonies based on coral species and picoplankton functional group. Genes characteristic of surface‐attached and potentially virulent microbial lifestyles were enriched in near‐coral seawater compared to reef seawater. There was a prominent association between the coral Porites astreoides and the coral symbiont Endozoicomonas, suggesting recruitment and/or shedding of these cells into the surrounding seawater. This evidence extends our understanding of potential species‐specific and reef site‐influenced microbial interactions that occur between corals and microorganisms within this near‐coral seawater environment that we propose to call the “coral ecosphere.” Microbial interactions that occur within the coral ecosphere could influence recruitment of coral‐associated microorganisms and facilitate the transfer of coral metabolites into the microbial food web, thus fostering reef biogeochemical cycling and a linkage between corals and the water column.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionsupporting

confidence: 70%

Section: Methodsmentioning

confidence: 99%

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The coral ecosphere: A unique coral reef habitat that fosters coral–microbial interactions

Weber

González‐Díaz

Armenteros

et al. 2019

Limnology & Oceanography

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“…Aspects of coral biology also influence microbiome structure and function. Similar to humans, compartmentalization of the microbiome generates distinct microbial communities in the coral animal, within the surface mucus layer, tissues, skeleton, and gut (Sweet et al, 2010;Ainsworth et al, 2015;Apprill et al, 2016) and some particularly associated with Symbiodinium (Ainsworth et al, 2015). Coral-associated bacteria can be transferred vertically from parent to larva (Sharp et al, 2012) or they can be horizontally acquired from the environment (Apprill et al, 2009;Sharp et al, 2010), including when adult corals release bacteria (e.g., Altermonas and Roseobacter) as a by-product of broadcast spawning (Ceh et al, 2013b).…”

Section: Introductionmentioning

confidence: 99%

Responses of Coral-Associated Bacterial Communities to Local and Global Stressors

et al. 2017

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The microbial contribution to ecological resilience is still largely overlooked in coral reef ecology. Coral-associated bacteria serve a wide variety of functional roles with reference to the coral host, and thus, the composition of the overall microbiome community can strongly influence coral health and survival. Here, we synthesize the findings of recent studies (n = 45) that evaluated the impacts of the top three stressors facing coral reefs (climate change, water pollution and overfishing) on coral microbiome community structure and diversity. Contrary to the species losses that are typical of many ecological communities under stress, here we show that microbial richness tends to be higher rather than lower for stressed corals (i.e., in ∼60% of cases), regardless of the stressor. Microbial responses to stress were taxonomically consistent across stressors, with specific taxa typically increasing in abundance (e.g

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“…Seasonality is reflected both in the coral physiology (Crossland, 1984;Warner et al, 2002;Ulstrup et al, 2008) and in the composition of coral-associated microbial communities (Brown et al, 1999;Fitt et al, 2000;Littman et al, 2010;Li et al, 2014). The symbiotic association of the coral animal with its diverse assemblages of microorganisms consisting in bacteria, archaea, fungi, viruses, and protists, including the dinoflagellate algae Symbiodinium (Kelly et al, 2014;Apprill et al, 2016), is termed the coral holobiont (Rohwer et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Ultra-Violet Radiation Has a Limited Impact on Seasonal Differences in the Acropora Muricata Holobiont

et al. 2018

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Environmental conditions are known to influence corals and their associated communities of microorganisms. However, our insights into the impacts of seasonal changes in ultraviolet radiation (UVR) on both coral physiology and microbiome remain very limited. To address this challenge, we maintained the coral Acropora muricata shaded from UVR or under ambient UVR levels during two contrasting seasons, i.e. summer and winter, and assessed the impact of UVR on the coral holobiont at each season. To this end, we analyzed the physiology (e.g., calcification, protein content, photosynthesis-related parameters) and coral microbiota composition, as well as the abundance and composition of the microbial communities and organic matter contents of the surrounding seawater. Our results show major seasonal effects on coral phenotype: (1) a lower host biomass and photosynthesizing, but fast calcifying phenotype in summer, and (2) a higher host biomass and photosynthesizing, but slow calcifying phenotype in winter. UVR had only a significant impact on Symbiodinium functioning. Specifically, high UVR levels reduced photosynthesis efficiency in summer, but an increase in chlorophyll a content may have compensated for this effect. The coral microbiota, which was variable but generally dominated by Endozoicomonas, was not affected by UVR, but its composition differed between seasons. In contrast, UVR had a major, but differential impact on the seawater microbial communities at both seasons. Particularly in summer, bacteria from the Alteromonadaceae were significantly more abundant (15-fold; up to 75%) in seawater under ambient UVR levels. Overall, our study suggests that UVR has only a limited impact on coral holobiont composition and functioning, despite major fluctuations in the surrounding seawater microbiome; seasonal changes in the holobiont are thus mostly driven by other environmental factors.

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Distinguishing between Microbial Habitats Unravels Ecological Complexity in Coral Microbiomes

Cited by 99 publications

References 71 publications

The coral ecosphere: A unique coral reef habitat that fosters coral–microbial interactions

The coral ecosphere: A unique coral reef habitat that fosters coral–microbial interactions

Responses of Coral-Associated Bacterial Communities to Local and Global Stressors

Ultra-Violet Radiation Has a Limited Impact on Seasonal Differences in the Acropora Muricata Holobiont

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