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Insights Into the Cultured Bacterial Fraction of Corals Insights into the cultured bacterial fraction of corals Michael Sweet ( [email protected] ) University of Derby https://orcid.org/0000-0003-4983-8333 Helena Villela Federal University of Rio de Janeiro Tina Keller-Costa Institute for Bioengineering and Biosciences Rodrigo Costa University of Lisbon https://orcid.org/0000-0002-5932-4101 Stefano Romano The Quadram Institute Bioscience https://orcid.org/0000-0002-7600-1953 David Bourne James Cook University Anny Cardenas University of Konstanz Megan Huggett The University of Newcastle, 10 Chittaway Rd, Ourimbah 2258 NSW Australia https://orcid.org/0000- 0002-3401-0704 Allison Kerwin McDaniel College, Westminster Felicity Kuek Pennsylvania State University Monica Medina Pennsylvania State University Julie Meyer Genetics Institute, University of Florida https://orcid.org/0000-0003-3382-3321 Moritz Müller Swinburne University of Technology Sarawak Campus https://orcid.org/0000-0001-8485-1598 Joseph Pollock Pennsylvania State University Michael Rappé University of Hawaii at Manoa Mathieu Sere University of Derby Koty Sharp Roger Williams University Christian Voolstra University of Konstanz https://orcid.org/0000-0003-4555-3795 Maren Ziegler Justus Liebig University Giessen Raquel Peixoto University of California, Davis https://orcid.org/0000-0002-9536-3132 Article Keywords: symbiosis, holobiont, metaorganism, cultured microorganisms, coral, probiotics, benecial microbes Posted Date: November 21st, 2020 DOI: https://doi.org/10.21203/rs.3.rs-105866/v1 License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License 1 Insights into the cultured bacterial fraction of corals 2 Sweet, Michael1*#; Villela, Helena2*; Keller-Costa, Tina3*; Costa, Rodrigo3,4*; Romano, 3 Stefano5*; Bourne, David G.6; Cárdenas, Anny7; Huggett, Megan J.8,9; Kerwin, Allison H.10; 4 Kuek, Felicity11; Medina, Mónica11; Meyer, Julie L.12; Müller, Moritz13; Pollock, F. Joseph.11,14, 5 Rappé, Michael S.15; Sere, Mathieu1; Sharp, Koty H.16; Voolstra, Christian R.7; Zaccardi, 6 Nathan16, Ziegler, Maren17; Peixoto, Raquel2,18,19* 7 1Aquatic Research Facility, Environmental Sustainability Research Centre, University of Derby, DE22 1GB, UK 8 2Federal University of Rio de Janeiro, Brazil 9 3Institute for Bioengineering and Biosciences (iBB), Instituto Superior Técnico (IST), University of Lisbon, 1049-001 Lisbon, 10 Portugal 11 4Department of Energy – Joint Genome Institute and Lawrence Berkeley National Laboratory, Berkeley, California 94720, 12 USA 13 5Gut Microbes and Health, Quadram Institute Bioscience, Norwich, NR4 7UQ, UK 14 6College of Science and Engineering, James Cook University and Australian Institute of Marine Science, Townsville, 4810, 15 Australia 16 7Department of Biology, University of Konstanz, Konstanz, Germany 17 8School of Environmental and Life Sciences, The University of Newcastle, 10 Chittaway Rd, Ourimbah 2258 NSW Australia 18 9Centre for Marine Ecosystems Research, Edith Cowan University, 270 Joondalup Dr, Joondalup 6027 WA Australia 19 10Department of Biology, McDaniel College, Westminster, MD, 21157, USA 20 11Department of Biology, Pennsylvania State University, University Park, PA 16802 21 12Soil and Water Sciences Department, Genetics Institute, University of Florida, Gainesville, FL, USA 22 13Faculty of Engineering, Computing and Science, Swinburne University of Technology Sarawak Campus, 93350 Kuching, 23 Sarawak, Malaysia. 24 14Hawaii and Palmyra Programs, The Nature Conservancy, 923 Nu`uanu Avenue, Honolulu, HI 96817 25 15Hawaii Institute of Marine Biology, University of Hawaii, P.O. Box 1346, Kaneohe, HI, 96744, USA 26 16Department of Biology and Marine Biology, Roger Williams University, Bristol, RI, 02809, USA 27 17Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Giessen, Germany 28 18IMAM-AquaRio – Rio de Janeiro Aquarium Research Center, Rio de Janeiro, Brazil. 29 19Genome Center, University of California Davis, USA. 30 *Authors contributed equally 31 #corresponding author: [email protected] 32 33 1 34 Abstract 35 Bacteria associated with coral hosts are diverse and abundant, with recent studies suggesting 36 involvement of these symbionts in host resilience to anthropogenic stress. Despite the 37 putative importance of bacteria, the work dedicated to culturing coral-associated bacteria 38 has received little attention. Combining published and unpublished data, here we report a 39 comprehensive overview of the diversity and function of culturable, coral-associated 40 bacteria. A total of 3055 isolates from 52 studies were considered by our meta-survey. Of 41 these, 1045 had full length 16S rRNA gene sequences, spanning 138 formally described and 42 12 putatively novel bacterial genera across the Proteobacteria, Firmicutes, Bacteroidetes, and 43 Actinobacteria phyla. We performed comparative genomic analysis using the available 44 genomes of 74 strains and identified potential signatures of beneficial bacterial-coral 45 symbioses among them. Our analysis revealed >400 biosynthetic gene clusters that underlie 46 the biosynthesis of antioxidant, antimicrobial, cytotoxic, and other secondary metabolites. 47 Moreover, we uncovered genomic features - not previously described for coral-bacterial 48 symbioses - involved in host colonization and host-symbiont recognition, antiviral defence 49 mechanisms, and/or integrated metabolic interactions, which we suggest as novel targets for 50 the screening of coral probiotics. Our results highlight the importance of bacterial cultures to 51 elucidate coral holobiont functioning, and guide the selection of probiotic candidates to 52 promote coral resilience and improve reef restoration efforts. 53 KEY WORDS: symbiosis, holobiont, metaorganism, cultured microorganisms, coral, probiotics, 54 beneficial microbes 55 Introduction 56 In recent years, the concept of the metaorganism or ‘holobiont’ has become a cornerstone of 57 biology 1, although the view of the holobiont as the unit of selection is a matter of current 58 debate 2. Notwithstanding, the term metaorganism has gained momentum in modern studies 59 of complex host-microbe interactions, as it defines the association formed by a host organism 60 and its microbiome 2,3,4. Scleractinian corals are an excellent example of such an association, 61 as they build reefs through close symbiotic interactions between the host modular animal, its 62 endosymbiotic dinoflagellates (Symbiodiniaceae) and an array of other microbial partners 2 63 including bacteria, archaea and fungi 1. The bacterial taxa associated with corals can vary 64 between coral species and geographical origin, though often there are patterns in the 65 community structure that link microbial and coral taxa 5,6. The majority of recent studies 66 exploring the importance of coral-associated microbes have focused on the use of cultivation- 67 independent approaches, based on 16S rRNA gene amplicon sequencing 7 and, more recently, 68 shotgun metagenomics 8. Such methods are central in identifying what bacteria are 69 associated with corals and how their metabolic and functional potential contribute to 70 holobiont health and response to environmental conditions 7,9 10. However, the bacterial 71 metabolic pathways that interact with the host and respond to environmental changes are 72 often best understood using culture-based approaches 11. This is particularly relevant because 73 metagenomic information gives insights into potential functional traits and other cellular 74 traits only, and often environmental changes have pleiotropic effects on holobiont physiology 75 that are impossible to grasp using metagenomics alone 12,13,14,15. 76 Inherently, culture-based approaches retrieve only a small fraction of the total bacterial 77 diversity within any given environment, a phenomenon known as the “great plate anomaly” 78 16,17,18. Often however, it is not a case of being ‘unculturable’, but of not yet knowing the range 79 of conditions needed to culture these microorganisms. Cultivating host-associated 80 microorganisms can be challenging, as their nutrient requirements and cross-feeding 81 networks are often unknown 19. In addition, many environmental microorganisms grow very 82 slowly (in contrast to clinical isolates), and are not adapted or capable of growing on 83 commonly used nutrient-rich media 20,21. To counter this, at least to some degree, recent 84 studies have implemented novel and alternative culture-based methods to retrieve a higher 85 proportion of the bacterial diversity in any given sample 19,22, and these approaches have also 86 been applied to corals 23,24,25. 87 Tissue compartmentalization and organismal complexity are thought to underlie high 88 bacterial diversity in corals 26,27,28. The diverse coral bacteriome plays an integral role in the 89 balance between health and disease of the coral holobiont 29 and represents a valuable source 90 of biotechnological products 30. 31 was perhaps the first to actively isolate bacteria from coral, 91 recovering strains from the skeletal regions of Porites lobata followed by 32 who reported on 92 bacteria isolated from mucus of Porites astreoides and two soft coral species. Microbial 93 mediated diseases have also been well documented as driving declines in reef health, 3 94 especially throughout the Caribbean for example 33. This has fostered a great interest in 95 understanding coral disease causative agents, stimulating cultivation efforts of coral- 96 associated bacteria 34,35,36. For example,
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