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Bacterial community dynamics are linked to patterns of coral heat tolerance.

ABSTRACT: Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposing these corals to thermal bleaching conditions changes the microbiome for heat-sensitive corals, but not for heat-tolerant corals growing in habitats with natural high heat extremes. Importantly, particular bacterial taxa predict the coral host response in a short-term heat stress experiment. Such associations could result from parallel responses of the coral and the microbial community to living at high natural temperatures. A competing hypothesis is that the microbial community and coral heat tolerance are causally linked.

SUBMITTER: Ziegler M

PROVIDER: S-EPMC5309854 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Bacterial community dynamics are linked to patterns of coral heat tolerance.

Ziegler Maren M Seneca Francois O FO Yum Lauren K LK Palumbi Stephen R SR Voolstra Christian R CR

Nature communications 20170210

Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposin ...[more]

PMID: 28186132

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Project description:Plants interact with complex microbial communities in which microorganisms play different roles in plant development and health. While certain microorganisms may cause disease, others promote nutrient uptake and resistance to stresses through a variety of mechanisms. Developing plant protection measures requires a deeper comprehension of the factors that influence multitrophic interactions and the organization of phyllospheric communities. High-throughput sequencing was used in this work to investigate the effects of climate variables and bacterial wildfire disease on the bacterial community's composition and assembly in the phyllosphere of tobacco (Nicotiana tabacum L.). The samples from June (M1), July (M2), August (M3), and September (M4) formed statistically separate clusters. The assembly of the whole bacterial population was mostly influenced by stochastic processes. PICRUSt2 predictions revealed genes enriched in the M3, a period when the plant wildfire disease index reached climax, were associated with the development of the wildfire disease (secretion of virulence factor), the enhanced metabolic capacity and environmental adaption. The M3 and M4 microbial communities have more intricate molecular ecological networks (MENs), bursting with interconnections within a densely networked bacterial population. The relative abundances of plant-beneficial and antagonistic microbes Clostridiales, Bacillales, Lactobacillales, and Sphingobacteriales, showed significant decrease in severally diseased sample (M3) compared to the pre-diseased samples (M1/M2). Following the results of MENs, we further test if the correlating bacterial pairs within the MEN have the possibility to share functional genes and we have unraveled 139 entries of such horizontal gene transfer (HGT) events, highlighting the significance of HGT in shaping the adaptive traits of plant-associated bacteria across the MENs, particularly in relation to host colonization and pathogenicity.

Project description:BackgroundMicrobiome 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.ResultsRecipients 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 these transmitted bacteria belonged to known, putatively symbiotic bacterial taxa of corals and were linked to the observed beneficial effect on the coral stress response. Microbiome dynamics in our experiments support the notion that microbiome community evenness and dominance of one or few bacterial species, rather than host-species identity, were drivers for microbiome stability in a holobiont context.ConclusionsOur results suggest that coral recipients likely favor the uptake of putative bacterial symbionts, recommending to include these taxonomic groups in future coral probiotics screening efforts. Our study suggests a scenario where these donor-specific bacterial symbionts might have been more efficient in supporting the recipients to resist heat stress compared to the native symbionts present in the control group. These findings urgently call for further experimental investigation of the mechanisms of action underlying the beneficial effect of CMT and for field-based long-term studies testing the persistence of the effect. Video abstract.

Project description:BackgroundStony corals provide the structural foundation of coral reef ecosystems and are termed holobionts given they engage in symbioses, in particular with photosynthetic dinoflagellates of the genus Symbiodinium. Besides Symbiodinium, corals also engage with bacteria affecting metabolism, immunity, and resilience of the coral holobiont, but the role of associated viruses is largely unknown. In this regard, the increase of studies using RNA sequencing (RNA-Seq) to assess gene expression provides an opportunity to elucidate viral signatures encompassed within the data via careful delineation of sequence reads and their source of origin.ResultsHere, we re-analyzed an RNA-Seq dataset from a cultured coral symbiont (Symbiodinium microadriaticum, Clade A1) across four experimental treatments (control, cold shock, heat shock, dark shock) to characterize associated viral diversity, abundance, and gene expression. Our approach comprised the filtering and removal of host sequence reads, subsequent phylogenetic assignment of sequence reads of putative viral origin, and the assembly and analysis of differentially expressed viral genes. About 15.46% (123 million) of all sequence reads were non-host-related, of which <1% could be classified as archaea, bacteria, or virus. Of these, 18.78% were annotated as virus and comprised a diverse community consistent across experimental treatments. Further, non-host related sequence reads assembled into 56,064 contigs, including 4856 contigs of putative viral origin that featured 43 differentially expressed genes during heat shock. The differentially expressed genes included viral kinases, ubiquitin, and ankyrin repeat proteins (amongst others), which are suggested to help the virus proliferate and inhibit the algal host's antiviral response.ConclusionOur results suggest that a diverse viral community is associated with coral algal endosymbionts of the genus Symbiodinium, which prompts further research on their ecological role in coral health and resilience.

Dataset Information

Bacterial community dynamics are linked to patterns of coral heat tolerance.

Publications

Bacterial community dynamics are linked to patterns of coral heat tolerance.

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