Contrasting Microbiome Dynamics of Putative Denitrifying Bacteria in Two Octocoral Species Exposed to Dissolved Organic Carbon (DOC) and Warming

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2022
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Hassenrück, Christiane
Simancas-Giraldo, Susana Marcela
Wild, Christian
Gärdes, Astrid
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Applied and Environmental Microbiology. American Society for Microbiology (ASM). 2022, 88(2), e01886-21. ISSN 0099-2240. eISSN 1098-5336. Available under: doi: 10.1128/AEM.01886-21
Zusammenfassung

Mutualistic nutrient cycling in the coral-algae symbiosis depends on limited nitrogen (N) availability for algal symbionts. Denitrifying prokaryotes capable of reducing nitrate or nitrite to dinitrogen could thus support coral holobiont functioning by limiting N availability. Octocorals show some of the highest denitrification rates among reef organisms; however, little is known about the community structures of associated denitrifiers and their response to environmental fluctuations. Combining 16S rRNA gene amplicon sequencing with nirS in-silico PCR and quantitative PCR, we found differences in bacterial community dynamics between two octocorals exposed to excess dissolved organic carbon (DOC) and concomitant warming. Although bacterial communities of the gorgonian Pinnigorgia flava remained largely unaffected by DOC and warming, the soft coral Xenia umbellata exhibited a pronounced shift toward Alphaproteobacteria dominance under excess DOC. Likewise, the relative abundance of denitrifiers was not altered in P. flava but decreased by 1 order of magnitude in X. umbellata under excess DOC, likely due to decreased proportions of Ruegeria spp. Given that holobiont C:N ratios remained stable in P. flava but showed a pronounced increase with excess DOC in X. umbellata, our results suggest that microbial community dynamics may reflect the nutritional status of the holobiont. Hence, denitrifier abundance may be directly linked to N availability. This suggests a passive regulation of N cycling microbes based on N availability, which could help stabilize nutrient limitation in the coral-algal symbiosis and thereby support holobiont functioning in a changing environment. IMPORTANCE Octocorals are important members of reef-associated benthic communities that can rapidly replace scleractinian corals as the dominant ecosystem engineers on degraded reefs. Considering the substantial change in the (a)biotic environment that is commonly driving reef degradation, maintaining a dynamic and metabolically diverse microbial community might contribute to octocoral acclimatization. Nitrogen (N) cycling microbes, in particular denitrifying prokaryotes, may support holobiont functioning by limiting internal N availability, but little is known about the identity and (a)biotic drivers of octocoral-associated denitrifiers. Here, we show contrasting dynamics of bacterial communities associated with two common octocoral species, the soft coral Xenia umbellata and the gorgonian Pinnigorgia flava after a 6-week exposure to excess dissolved organic carbon under concomitant warming conditions. The specific responses of denitrifier communities of the two octocoral species aligned with the nutritional status of holobiont members. This suggests a passive regulation based on N availability in the coral holobiont.

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570 Biowissenschaften, Biologie
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nitrogen limitation, denitrification, microbial plasticity, Symbiodiniaceaebacteria interactions, phase shifts
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ISO 690XIANG, Nan, Christiane HASSENRÜCK, Claudia POGOREUTZ, Nils RÄDECKER, Susana Marcela SIMANCAS-GIRALDO, Christian R. VOOLSTRA, Christian WILD, Astrid GÄRDES, 2022. Contrasting Microbiome Dynamics of Putative Denitrifying Bacteria in Two Octocoral Species Exposed to Dissolved Organic Carbon (DOC) and Warming. In: Applied and Environmental Microbiology. American Society for Microbiology (ASM). 2022, 88(2), e01886-21. ISSN 0099-2240. eISSN 1098-5336. Available under: doi: 10.1128/AEM.01886-21
BibTex
@article{Xiang2022-01-25Contr-56669,
  year={2022},
  doi={10.1128/AEM.01886-21},
  title={Contrasting Microbiome Dynamics of Putative Denitrifying Bacteria in Two Octocoral Species Exposed to Dissolved Organic Carbon (DOC) and Warming},
  number={2},
  volume={88},
  issn={0099-2240},
  journal={Applied and Environmental Microbiology},
  author={Xiang, Nan and Hassenrück, Christiane and Pogoreutz, Claudia and Rädecker, Nils and Simancas-Giraldo, Susana Marcela and Voolstra, Christian R. and Wild, Christian and Gärdes, Astrid},
  note={Article Number: e01886-21}
}
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    <dcterms:abstract xml:lang="eng">Mutualistic nutrient cycling in the coral-algae symbiosis depends on limited nitrogen (N) availability for algal symbionts. Denitrifying prokaryotes capable of reducing nitrate or nitrite to dinitrogen could thus support coral holobiont functioning by limiting N availability. Octocorals show some of the highest denitrification rates among reef organisms; however, little is known about the community structures of associated denitrifiers and their response to environmental fluctuations. Combining 16S rRNA gene amplicon sequencing with nirS in-silico PCR and quantitative PCR, we found differences in bacterial community dynamics between two octocorals exposed to excess dissolved organic carbon (DOC) and concomitant warming. Although bacterial communities of the gorgonian Pinnigorgia flava remained largely unaffected by DOC and warming, the soft coral Xenia umbellata exhibited a pronounced shift toward Alphaproteobacteria dominance under excess DOC. Likewise, the relative abundance of denitrifiers was not altered in P. flava but decreased by 1 order of magnitude in X. umbellata under excess DOC, likely due to decreased proportions of Ruegeria spp. Given that holobiont C:N ratios remained stable in P. flava but showed a pronounced increase with excess DOC in X. umbellata, our results suggest that microbial community dynamics may reflect the nutritional status of the holobiont. Hence, denitrifier abundance may be directly linked to N availability. This suggests a passive regulation of N cycling microbes based on N availability, which could help stabilize nutrient limitation in the coral-algal symbiosis and thereby support holobiont functioning in a changing environment. IMPORTANCE Octocorals are important members of reef-associated benthic communities that can rapidly replace scleractinian corals as the dominant ecosystem engineers on degraded reefs. Considering the substantial change in the (a)biotic environment that is commonly driving reef degradation, maintaining a dynamic and metabolically diverse microbial community might contribute to octocoral acclimatization. Nitrogen (N) cycling microbes, in particular denitrifying prokaryotes, may support holobiont functioning by limiting internal N availability, but little is known about the identity and (a)biotic drivers of octocoral-associated denitrifiers. Here, we show contrasting dynamics of bacterial communities associated with two common octocoral species, the soft coral Xenia umbellata and the gorgonian Pinnigorgia flava after a 6-week exposure to excess dissolved organic carbon under concomitant warming conditions. The specific responses of denitrifier communities of the two octocoral species aligned with the nutritional status of holobiont members. This suggests a passive regulation based on N availability in the coral holobiont.</dcterms:abstract>
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