Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny

Pollock, F. Joseph; McMinds, Ryan; Smith, S.J.; Bourne, David G.; Willis, Bette L.; Medina, Mónica; Thurber, Rebecca Vega; Zaneveld, Jesse

doi:10.1038/s41467-018-07275-x

Cited by 297 publications

(355 citation statements)

References 59 publications

(70 reference statements)

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“…In addition, photographic survey results showed little evidence of short‐term acclimatization. Interestingly, the abundance of two species of prokaryotes, Tepidiphilus and Endozoicomonas , differed among microbiome samples depending on their bleaching response and this supports findings that Endozoicomonas plays an important role in the functioning of the coral holobiont (Pollock et al, ). Ultradeep sequencing of host and symbionts may reveal the occurrence of somatic mutations in hosts (and/or symbionts) correlated with the bleaching phenotype (Van Oppen, Souter, Howells, Heyward, & Berkelmans, ) but nonmutation‐based mechanisms may also play a role (Goldsmith & Tawfik, ; Payne & Wagner, ), including detection‐based epigenetic modifications (sensu Shea, Pen, & Uller, ).…”

Section: Discussionsupporting

confidence: 80%

“…Corals associate with a diverse set of prokaryotes (Pollock et al, 2018). The microbiome plays important roles in the functioning of the holobiont, including coral nutrition, element cycling and disease responses (Peixoto, Rosado, Leite, Rosado, & Bourne, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…We are beginning to understand the specific function of some members of the microbiome such as an endosymbiotic cyanobacterium that fixes nitrogen in Montastraea cavernosa (Lesser et al, 2007) and the disease-causing Vibrio corallyticus (Kimes et al, 2012). Other species, such as Endozoicomonas sp., show patterns of association with coral hosts that suggest an important role, but that role is not yet well understood (Neave et al, 2017;Pollock et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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What drives phenotypic divergence among coral clonemates of Acropora palmata?

et al. 2019

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Evolutionary rescue of populations depends on their ability to produce phenotypic variation that is heritable and adaptive. DNA mutations are the best understood mechanisms to create phenotypic variation, but other, less well‐studied mechanisms exist. Marine benthic foundation species provide opportunities to study these mechanisms because many are dominated by isogenic stands produced through asexual reproduction. For example, Caribbean acroporid corals are long lived and reproduce asexually via breakage of branches. Fragmentation is often the dominant mode of local population maintenance. Thus, large genets with many ramets (colonies) are common. Here, we observed phenotypic variation in stress responses within genets following the coral bleaching events in 2014 and 2015 caused by high water temperatures. This was not due to genetic variation in their symbiotic dinoflagellates (Symbiodinium “fitti”) because each genet of this coral species typically harbours a single strain of S. “fitti”. Characterization of the microbiome via 16S tag sequencing correlated the abundance of only two microbiome members (Tepidiphilus, Endozoicomonas) with a bleaching response. Epigenetic changes were significantly correlated with the host's genetic background, the location of the sampled polyps within the colonies (e.g., branch vs. base of colony), and differences in the colonies’ condition during the bleaching event. We conclude that long‐term microenvironmental differences led to changes in the way the ramets methylated their genomes, contributing to the differential bleaching response. However, most of the variation in differential bleaching response among clonemates of Acropora palmata remains unexplained. This research provides novel data and hypotheses to help understand intragenet variability in stress phenotypes of sessile marine species.

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Section: Discussionsupporting

confidence: 80%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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What drives phenotypic divergence among coral clonemates of Acropora palmata?

et al. 2019

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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%

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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“…However, phylosymbiosis is agnostic to mechanism. Additional methods exist for determining the relationship between host phylogeny and the microbiome (e.g., using simulations in Mazel et al, 2018; Mantel tests in Pollock et al, 2018; multiple regression tests in Youngblut et al, 2019); however, the evolutionary processes that generate the microbiome have been relatively unexplored. Here, we proposed utilizing the microbiome as a trait of a host (Benson, 2016;Benson et al, 2010), and extrapolating that trait to host species.…”

mentioning

confidence: 99%

Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea

et al. 2020

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How the microbiome interacts with hosts across evolutionary time is poorly understood. Data sets including many host species are required to conduct comparative analyses. Here, we analyzed 142 intestinal microbiome samples from 92 birds belonging to 74 species from Equatorial Guinea, using the 16S rRNA gene. Using four definitions for microbial taxonomic units (97%OTU, 99%OTU, 99%OTU with singletons removed, ASV), we conducted alpha and beta diversity analyses. We found that raw abundances and diversity varied between the data sets but relative patterns were largely consistent across data sets. Host taxonomy, diet and locality were significantly associated with microbiomes, at generally similar levels using three distance metrics. Phylogenetic comparative methods assessed the evolutionary relationship between the microbiome as a trait of a host species and the underlying bird phylogeny. Using multiple ways of defining “microbiome traits”, we found that a neutral Brownian motion model did not explain variation in microbiomes. Instead, we found a White Noise model (indicating little phylogenetic signal), was most likely. There was some support for the Ornstein‐Uhlenbeck model (that invokes selection), but the level of support was similar to that of a White Noise simulation, further supporting the White Noise model as the best explanation for the evolution of the microbiome as a trait of avian hosts. Our study demonstrated that both environment and evolution play a role in the gut microbiome and the relationship does not follow a neutral model; these biological results are qualitatively robust to analytical choices.

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Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny

Cited by 297 publications

References 59 publications

What drives phenotypic divergence among coral clonemates of Acropora palmata?

What drives phenotypic divergence among coral clonemates of Acropora palmata?

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

Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea

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