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Dynamics of coral-associated microbiomes during a thermal bleaching event.

ABSTRACT: Coral-associated microorganisms play an important role in their host fitness and survival. A number of studies have demonstrated connections between thermal tolerance in corals and the type/relative abundance of Symbiodinium they harbor. More recently, the shifts in coral-associated bacterial profiles were also shown to be linked to the patterns of coral heat tolerance. Here, we investigated the dynamics of Porites lutea-associated bacterial and algal communities throughout a natural bleaching event, using full-length 16S rRNA and internal transcribed spacer sequences (ITS) obtained from PacBio circular consensus sequencing. We provided evidence of significant changes in the structure and diversity of coral-associated microbiomes during thermal stress. The balance of the symbiosis shifted from a predominant association between corals and Gammaproteobacteria to a predominance of Alphaproteobacteria and to a lesser extent Betaproteobacteria following the bleaching event. On the contrary, the composition and diversity of Symbiodinium communities remained unaltered throughout the bleaching event. It appears that the switching and/or shuffling of Symbiodinium types may not be the primary mechanism used by P. lutea to cope with increasing seawater temperature. The shifts in the structure and diversity of associated bacterial communities may contribute more to the survival of the coral holobiont under heat stress.

SUBMITTER: Pootakham W

PROVIDER: S-EPMC6182559 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Dynamics of coral-associated microbiomes during a thermal bleaching event.

Pootakham Wirulda W Mhuantong Wuttichai W Putchim Lalita L Yoocha Thippawan T Sonthirod Chutima C Kongkachana Wasitthee W Sangsrakru Duangjai D Naktang Chaiwat C Jomchai Nukoon N Thongtham Nalinee N Tangphatsornruang Sithichoke S

MicrobiologyOpen 20180323 5

Coral-associated microorganisms play an important role in their host fitness and survival. A number of studies have demonstrated connections between thermal tolerance in corals and the type/relative abundance of Symbiodinium they harbor. More recently, the shifts in coral-associated bacterial profiles were also shown to be linked to the patterns of coral heat tolerance. Here, we investigated the dynamics of Porites lutea-associated bacterial and algal communities throughout a natural bleaching e ...[more]

PMID: 29573244

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Project description:The thermal bleaching percentage of coral holobionts shows interspecific differences under heat-stress conditions, which are closely related to the coral-associated microbiome. However, the ecological effects of community dynamics and interactions between Symbiodiniaceae and fungi on coral thermal bleaching susceptibility remain unclear. In this study, we analyzed the diversity, community structure, functions, and potential interaction of Symbiodiniaceae and fungi among 18 coral species from a high thermal bleaching risk atoll using next-generation sequencing. The results showed that heat-tolerant C3u sub-clade and Durusdinium dominated the Symbiodiniaceae community of corals and that there were no core amplicon sequence variants in the coral-associated fungal community. Fungal richness and the abundance of confirmed functional animal-plant pathogens were significantly positively correlated with the coral thermal bleaching percentage. Fungal indicators, including Didymellaceae, Chaetomiaceae, Schizophyllum, and Colletotrichum, were identified in corals. Each coral species had a complex Symbiodiniaceae-fungi interaction network (SFIN), which was driven by the dominant Symbiodiniaceae sub-clades. The SFINs of coral holobionts with low thermal bleaching susceptibility exhibited low complexity and high betweenness centrality. These results indicate that the extra heat tolerance of coral in Huangyan Island may be linked to the high abundance of heat-tolerant Symbiodiniaceae. Fungal communities have high interspecific flexibility, and the increase of fungal diversity and pathogen abundance was correlated with higher thermal bleaching susceptibility of corals. Moreover, fungal indicators were associated with the degrees of coral thermal bleaching susceptibility, including both high and intermediate levels. The topological properties of SFINs suggest that heat-tolerant coral have limited fungal parasitism and strong microbial network resilience.IMPORTANCEGlobal warming and enhanced marine heatwaves have led to a rapid decline in coral reef ecosystems worldwide. Several studies have focused on the impact of coral-associated microbiomes on thermal bleaching susceptibility in corals; however, the ecological functions and interactions between Symbiodiniaceae and fungi remain unclear. We investigated the microbiome dynamics and potential interactions of Symbiodiniaceae and fungi among 18 coral species in Huangyan Island. Our study found that the Symbiodiniaceae community of corals was mainly composed of heat-tolerant C3u sub-clade and Durusdinium. The increase in fungal diversity and pathogen abundance has close associations with higher coral thermal bleaching susceptibility. We first constructed an interaction network between Symbiodiniaceae and fungi in corals, which indicated that restricting fungal parasitism and strong interaction network resilience would promote heat acclimatization of corals. Accordingly, this study provides insights into the role of microorganisms and their interaction as drivers of interspecific differences in coral thermal bleaching.

Project description:As coral bleaching events become more frequent and intense, our ability to predict and mitigate future events depends upon our capacity to interpret patterns within previous episodes. Responses to thermal stress vary among coral species; however the diversity of coral assemblages, environmental conditions, assessment protocols, and severity criteria applied in the global effort to document bleaching patterns creates challenges for the development of a systemic metric of taxon-specific response. Here, we describe and validate a novel framework to standardize bleaching response records and estimate their measurement uncertainties. Taxon-specific bleaching and mortality records (2036) of 374 coral taxa (during 1982-2006) at 316 sites were standardized to average percent tissue area affected and a taxon-specific bleaching response index (taxon-BRI) was calculated by averaging taxon-specific response over all sites where a taxon was present. Differential bleaching among corals was widely variable (mean taxon-BRI = 25.06 ± 18.44%, ±SE). Coral response may differ because holobionts are biologically different (intrinsic factors), they were exposed to different environmental conditions (extrinsic factors), or inconsistencies in reporting (measurement uncertainty). We found that both extrinsic and intrinsic factors have comparable influence within a given site and event (60% and 40% of bleaching response variance of all records explained, respectively). However, when responses of individual taxa are averaged across sites to obtain taxon-BRI, differential response was primarily driven by intrinsic differences among taxa (65% of taxon-BRI variance explained), not conditions across sites (6% explained), nor measurement uncertainty (29% explained). Thus, taxon-BRI is a robust metric of intrinsic susceptibility of coral taxa. Taxon-BRI provides a broadly applicable framework for standardization and error estimation for disparate historical records and collection of novel data, allowing for unprecedented accuracy in parameterization of mechanistic and predictive models and conservation plans.

Project description:BackgroundHigh sea surface temperatures resulted in widespread coral bleaching and mortality in Mayotte Island (northern Mozambique channel, Indian Ocean: 12.1°S, 45.1°E) in April-June 2010.MethodsTwenty three representative coral genera were sampled quantitatively for size class distributions during the peak of the bleaching event to measure its impact.ResultsFifty two percent of coral area was impacted, comprising 19.3% pale, 10.7% bleached, 4.8% partially dead and 17.5% recently dead. Acropora, the dominant genus, was the second most susceptible to bleaching (22%, pale and bleached) and mortality (32%, partially dead and dead), only exceeded by Pocillopora (32% and 47%, respectively). The majority of genera showed intermediate responses, and the least response was shown by Acanthastrea and Leptastrea (6% pale and bleached). A linear increase in bleaching susceptibility was found from small colonies (<2.5 cm, 83% unaffected) to large ones (>80 cm, 33% unaffected), across all genera surveyed. Maximum mortality in 2010 was estimated at 32% of coral area or biomass, compared to half that (16%), by colony abundance.DiscussionMayotte reefs have displayed a high level of resilience to bleaching events in 1983, 1998 and the 2010 event reported here, and experienced a further bleaching event in 2016. However, prospects for continued resilience are uncertain as multiple threats are increasing: the rate of warming experienced (0.1 °C per decade) is some two to three times less than projected warming in coming decades, the interval between severe bleaching events has declined from 16 to 6 years, and evidence of chronic mortality from local human impacts is increasing. The study produced four recommendations for reducing bias when monitoring and assessing coral bleaching: coral colony size should be measured, unaffected colonies should be included in counts, quadrats or belt transects should be used and weighting coefficients in the calculation of indices should be used with caution.

Dataset Information

Dynamics of coral-associated microbiomes during a thermal bleaching event.

Publications

Dynamics of coral-associated microbiomes during a thermal bleaching event.

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