Coral holobiont cues prime Endozoicomonas for a symbiotic lifestyle

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Type
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Authors
Pogoreutz, Claudia cc
Oakley, Clinton A cc
Rädecker, Nils cc
Cardenas, Anny cc
Perna, Gabriela cc
Xiang, Nan
Peng, Lifeng
Davy, Simon K. cc
Ngugi, David K.
Voolstra, Christian R. cc
KAUST Department
Biological and Environmental Science and Engineering (BESE) Division
Marine Science Program
Red Sea Research Center (RSRC)
Red Sea Research Center, Biological, Environmental, Science and Engineering, King Abdullah University of Science and Technology (KAUST), 23955, Thuwal, Saudi Arabia
Reef Genomics Lab
KAUST Grant Number
URF/1/3400-01-01
Date
2022-04-20
Permanent link to this record
http://hdl.handle.net/10754/676453

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Abstract
Endozoicomonas are prevalent, abundant bacterial associates of marine animals, including corals. Their role in holobiont health and functioning, however, remains poorly understood. To identify potential interactions within the coral holobiont, we characterized the novel isolate Endozoicomonas marisrubri sp. nov. 6c and assessed its transcriptomic and proteomic response to tissue extracts of its native host, the Red Sea coral Acropora humilis. We show that coral tissue extracts stimulated differential expression of genes putatively involved in symbiosis establishment via the modulation of the host immune response by E. marisrubri 6c, such as genes for flagellar assembly, ankyrins, ephrins, and serpins. Proteome analyses revealed that E. marisrubri 6c upregulated vitamin B1 and B6 biosynthesis and glycolytic processes in response to holobiont cues. Our results suggest that the priming of Endozoicomonas for a symbiotic lifestyle involves the modulation of host immunity and the exchange of essential metabolites with other holobiont members. Consequently, Endozoicomonas may play an important role in holobiont nutrient cycling and may therefore contribute to coral health, acclimatization, and adaptation.
Citation
Pogoreutz, C., Oakley, C. A., Rädecker, N., Cárdenas, A., Perna, G., Xiang, N., Peng, L., Davy, S. K., Ngugi, D. K., & Voolstra, C. R. (2022). Coral holobiont cues prime Endozoicomonas for a symbiotic lifestyle. The ISME Journal. https://doi.org/10.1038/s41396-022-01226-7
Sponsors
CP would like to thank Ramzi Al-Jadahli, Zenon B Batang, Nabeel M Alikunhi, and the boat crews of the Center for Marine Operations and Research (CMOR) at KAUST for support with fieldwork and coral husbandry. CP is grateful to Ana Flor Vidal for bacteriology and culturing support, Hai Wang for PacBio library preparation, Shuorug M Al Bihani and Luke Esau for flow cytometry support, Hagen M Gegner for field support during coral collection, Alyssa Bell for technical support, Rúben Martins da Costa for primer design, and Matthew J Neave and Jean-Baptiste Raina for fruitful discussions. This project was supported by KAUST baseline funds to CRV. The contribution of CP and NR was supported by KAUST Competitive Research Grant, award number URF/1/3400-01-01, to CP, NR, AC, and CRV. Further financial support for this research was provided through University of Konstanz AFF Funding (15902919 FP 029/19) to CP, NR, and CRV, an Independent Research Grant 2020 by the Center for Advanced Research at the University of Konstanz to CP, and by the Marsden Fund of the Royal Society Te Apārangi, award number 19-VUW-086, to SKD and CAO. NX acknowledges a scholarship by the China Scholarship Council (CSC, scholarship ID 201807565016). The mass spectrometry facility and proteomics data processing platform at the Victoria University of Wellington (VUW) are acknowledged. We thank David McLauchlan at VUW for maintaining the proteomics software and mass spectrometry data. Finally, the authors would like to thank two anonymous reviewers and the editors for their constructive feedback, which greatly improved the manuscript. Figures 1, 4, 5 were conceived by CP and created using BioRender.com
Open Access funding enabled and organized by Projekt DEAL
Publisher
Springer Science and Business Media LLC
Journal
The ISME Journal
DOI
10.1038/s41396-022-01226-7
PubMed ID
35444262
Additional Links
https://www.nature.com/articles/s41396-022-01226-7
Collections
Articles; Biological and Environmental Science and Engineering (BESE) Division; Red Sea Research Center (RSRC); Marine Science Program
Archived with thanks to The ISME Journal under a Creative Commons license, details at: https://creativecommons.org/licenses/by/4.0
Except where otherwise noted, this item's license is described as Archived with thanks to The ISME Journal under a Creative Commons license, details at: https://creativecommons.org/licenses/by/4.0