Insights into the Cultured Bacterial Fraction of Corals Item Type Article Authors Sweet, Michael; Villela, Helena; Keller-Costa, Tina; Costa, Rodrigo; Romano, Stefano; Bourne, David G.; Cárdenas, Anny; Huggett, Megan J.; Kerwin, Allison H.; Kuek, Felicity; Medina, Mónica; Meyer, Julie L.; Müller, Moritz; Pollock, F. Joseph; Rappé, Michael S.; Sere, Mathieu; Sharp, Koty H.; Voolstra, Christian R.; Zaccardi, Nathan; Ziegler, Maren; Peixoto, Raquel Citation Sweet, M., Villela, H., Keller-Costa, T., Costa, R., Romano, S., Bourne, D., Cardenas, A., Huggett, M., Kerwin, A., Kuek, F. Medina, M., et al. (2021). 'Insights into the cultured bacterial fraction of corals'. msystems, 6(3), pp. 1-18. DOI 10.1128/msystems.01249-20 Publisher American Society for Microbiology Journal msystems Download date 04/10/2021 02:15:55 Item License https://creativecommons.org/licenses/by/4.0/ Link to Item http://hdl.handle.net/10545/625844 RESEARCH ARTICLE Insights into the Cultured Bacterial Fraction of Corals Michael Sweet,a Helena Villela,b Tina Keller-Costa,c,d Rodrigo Costa,c,d,e Stefano Romano,f David G. Bourne,g,h Anny Cárdenas,i Megan J. Huggett,j,k Allison H. Kerwin,l Felicity Kuek,h,m Mónica Medina,n Julie L. Meyer,o Moritz Müller,p F. Joseph Pollock,n,q Michael S. Rappé,r Mathieu Sere,a Koty H. Sharp,s Christian R. Voolstra,i Nathan Zaccardi,s Maren Ziegler,t Raquel Peixotob,u aAquatic Research Facility, Environmental Sustainability Research Centre, University of Derby, Derby, United Kingdom bFederal University of Rio de Janeiro, Rio de Janeiro, Brazil cInstitute for Bioengineering and Biosciences (iBB), University of Lisbon, Lisbon, Portugal dInstituto Superior Técnico (IST), University of Lisbon, Lisbon, Portugal eDepartment of Energy, Joint Genome Institute and Lawrence Berkeley National Laboratory, Berkeley, California, USA fGut Microbes and Health, Quadram Institute Bioscience, Norwich, United Kingdom gCollege of Science and Engineering, James Cook University, Townsville, Australia hAustralian Institute of Marine Science, Townsville, Australia iDepartment of Biology, University of Konstanz, Konstanz, Germany jSchool of Environmental and Life Sciences, The University of Newcastle, Ourimbah, NSW, Australia kCentre for Marine Ecosystems Research, Edith Cowan University, Joondalup, WA, Australia lDepartment of Biology, McDaniel College, Westminster, Maryland, USA mCollege of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Australia nDepartment of Biology, Pennsylvania State University, University Park, Pennsylvania, USA oSoil and Water Sciences Department, Genetics Institute, University of Florida, Gainesville, Florida, USA pFaculty of Engineering, Computing and Science, Swinburne University of Technology Sarawak Campus, Kuching, Sarawak, Malaysia qHawaii and Palmyra Programs, The Nature Conservancy, Honolulu, Hawaii, USA rHawaii Institute of Marine Biology, University of Hawaii, Kaneohe, Hawaii, USA sDepartment of Biology and Marine Biology, Roger Williams University, Bristol, Rhode Island, USA tDepartment of Animal Ecology and Systematics, Justus Liebig University Giessen, Giessen, Germany uRed Sea Research Center (RSRC), Division of Biological and Environmental Science and Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia Michael Sweet, Helena Villela, Tina Keller-Costa, Rodrigo Costa, Stefano Romano, and Raquel Peixoto contributed equally. Author order was determined by mutual agreement. ABSTRACT Bacteria associated with coral hosts are diverse and abundant, with Citation Sweet M, Villela H, Keller-Costa T, Costa recent studies suggesting involvement of these symbionts in host resilience to R, Romano S, Bourne DG, Cárdenas A, Huggett anthropogenic stress. Despite their putative importance, the work dedicated to cultur- MJ, Kerwin AH, Kuek F, Medina M, Meyer JL, MüllerM,PollockFJ,RappéMS,SereM,SharpKH, ing coral-associated bacteria has received little attention. Combining published and Voolstra CR, Zaccardi N, Ziegler M, Peixoto R. unpublished data, here we report a comprehensive overview of the diversity and func- 2021. Insights into the cultured bacterial fraction of corals. mSystems 6:e01249-20. https://doi.org/ tion of culturable bacteria isolated from corals originating from tropical, temperate, and 10.1128/mSystems.01249-20. cold-water habitats. A total of 3,055 isolates from 52 studies were considered by our Editor Nick Bouskill, Lawrence Berkeley metasurvey. Of these, 1,045 had full-length 16S rRNA gene sequences, spanning 138 for- National Laboratory mally described and 12 putatively novel bacterial genera across the Proteobacteria, Ad Hoc Peer Reviewers Lauren Speare, University of North Carolina at Chapel Hill; Firmicutes, Bacteroidetes,andActinobacteria phyla. We performed comparative genomic Amanda Shore, Farmingdale State College analysis using the available genomes of 74 strains and identified potential signatures of Copyright © 2021 Sweet et al. This is an open- beneficial bacterium-coral symbioses among the strains. Our analysis revealed .400 bio- access article distributed under the terms of the Creative Commons Attribution 4.0 synthetic gene clusters that underlie the biosynthesis of antioxidant, antimicrobial, cyto- International license. toxic, and other secondary metabolites. Moreover, we uncovered genomic features—not Address correspondence to Michael Sweet, previously described for coral-bacterium symbioses—potentially involved in host coloni- [email protected], or Raquel Peixoto, [email protected]. zation and host-symbiont recognition, antiviral defense mechanisms, and/or integrated metabolic interactions, which we suggest as novel targets for the screening of coral Received 1 December 2020 Accepted 13 May 2021 probiotics. Our results highlight the importance of bacterial cultures to elucidate Published 22 June 2021 coral holobiont functioning and guide the selection of probiotic candidates to May/June 2021 Volume 6 Issue 3 e01249-20 msystems.asm.org 1 Downloaded from https://journals.asm.org/journal/msystems on 23 June 2021 by 86.21.88.225. Sweet et al. promotecoralresilienceandimproveholisticandcustomizedreefrestorationand rehabilitation efforts. IMPORTANCE Our paper is the first study to synthesize currently available but decen- tralized data of cultured microbes associated with corals. We were able to collate 3,055 isolates across a number of published studies and unpublished collections from various laboratories and researchers around the world. This equated to 1,045 individual isolates which had full-length 16S rRNA gene sequences, after filtering of the original 3,055. We also explored which of these had genomes available. Originally, only 36 were available, and as part of this study, we added a further 38— equating to 74 in total. From this, we investigated potential genetic signatures that may facilitate a host-associated lifestyle. Further, such a resource is an important step in the selection of probiotic candidates, which are being investigated for promoting coral resilience and potentially applied as a novel strategy in reef restoration and reha- bilitation efforts. In the spirit of open access, we have ensured this collection is available to the wider research community through the web site http://isolates.reefgenomics.org/ with the hope many scientists across the globe will ask for access to these cultures for future studies. KEYWORDS symbiosis, holobiont, metaorganism, cultured microorganisms, coral, probiotics, beneficial microbes, genomes, symbiosis n recent years, the concept of the metaorganism or holobiont, which defines the Iassociations formed by a host organism and its microbiome (1–3), has become a cor- nerstone of biology (4). Scleractinian corals are an excellent example of host-microbe associations, as they build reefs through close symbiotic interactions between the host modular animal, its endosymbiotic dinoflagellates (Symbiodiniaceae), and an array of other microbial partners, including bacteria, archaea, and fungi (3, 4). The bacterial taxa associated with corals can vary between coral species and geographical origin, though often there are patterns in the community structure that link microbial and coral taxa (5, 6). Many original discoveries on the importance of coral-associated bacte- ria and their interactions with the coral host were made using culture-based methods (7, 8). However, the majority of recent studies exploring the importance of coral-associ- ated microbes have focused on the use of cultivation-independent approaches, based on 16S rRNA gene amplicon sequencing (9) and, more recently, shotgun metagenom- ics (10, 11). Such methods are central in identifying what bacteria are associated with corals and how their metabolic and functional potential contribute to holobiont health and response to environmental conditions (9, 12–14). However, the bacterial metabolic pathways that interact with the host and respond to environmental changes are often best understood using culture-based approaches (15). This is particularly relevant because metagenomic information gives insights into potential functional traits and other cellular traits only, and often environmental changes have pleiotropic effects on holobiont physiology that are impossible to grasp using metagenomics alone (16–19). Inherently, culture-based approaches retrieve only a small fraction of the total bac- terial diversity within any given environment, a phenomenon known as the “great plate anomaly” (20–22). Often