Coral microbiomes as reservoirs of unknown genomic and biosynthetic diversity

Eddy, T. D. et al. Global decline in capacity of coral reefs to provide ecosystem services. One Earth 4, 1278–1285 (2021).Article  ADS  Google Scholar  Rocha, J., Peixe, L., Gomes, N. C. M. & Calado, R. Cnidarians as a source of new marine bioactive compounds—an overview of the last decade and future steps for bioprospecting. Mar. Drugs 9, 1860–1886 (2011).Article  PubMed  PubMed Central  CAS  Google Scholar  Planes, S. et al. The Tara Pacific expedition—a pan-ecosystemic approach of the ‘-omics’ complexity of coral reef holobionts across the Pacific Ocean. PLoS Biol. 17, e3000483 (2019).Article  PubMed  PubMed Central  CAS  Google Scholar  Smith, S. V. Coral-reef area and the contributions of reefs to processes and resources of the world’s oceans. Nature 273, 225–226 (1978).Article  ADS  Google Scholar  Fisher, R. et al. Species richness on coral reefs and the pursuit of convergent global estimates. Curr. Biol. 25, 500–505 (2015).Article  PubMed  CAS  Google Scholar  Knowlton, N. The future of coral reefs. Proc. Natl Acad. Sci. USA 98, 5419–5425 (2001).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Intergovernmental Panel on Climate Change (IPCC). Global Warming of 1.5 °C: IPCC Special Report on Impacts of Global Warming of 1.5 °C above Pre-industrial Levels in Context of Strengthening Response to Climate Change, Sustainable Development, and Efforts to Eradicate Poverty (eds Masson-Delmotte, V. et al.) (Cambridge Univ. Press, Cambridge, 2022).Rohwer, F., Seguritan, V., Azam, F. & Knowlton, N. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243, 1–10 (2002).Article  ADS  Google Scholar  Galand, P. E. et al. Diversity of the Pacific Ocean coral reef microbiome. Nat. Commun. 14, 3039 (2023).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Muscatine, L. & Porter, J. W. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27, 454–460 (1977).Article  Google Scholar  Voolstra, C. R. & Ziegler, M. Adapting with microbial help: microbiome flexibility facilitates rapid responses to environmental change. BioEssays 42, e2000004 (2020).Article  PubMed  Google Scholar  Ritchie, K. B. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322, 1–14 (2006).Article  ADS  CAS  Google Scholar  Kobayashi, M. et al. Marine natural products. XXXIV. Trisindoline, a new antibiotic indole trimer, produced by a bacterium of Vibrio sp. separated from the marine sponge Hyrtios altum. Chem. Pharm. Bull. 42, 2449–2451 (1994).Article  CAS  Google Scholar  Bertin, M. J. et al. Spongosine production by a Vibrio harveyi strain associated with the sponge Tectitethya crypta. J. Nat. Prod. 78, 493–499 (2015).Article  PubMed  PubMed Central  CAS  Google Scholar  Romero, F. et al. Thiocoraline, a new depsipeptide with antitumor activity produced by a marine Micromonospora. J. Antibiot. 50, 734–737 (1997).Article  CAS  Google Scholar  Blockley, A., Elliott, D. R., Roberts, A. P. & Sweet, M. Symbiotic microbes from marine invertebrates: driving a new era of natural product drug discovery. Diversity 9, 49 (2017).Article  Google Scholar  Newman, D. J. From large-scale collections to the potential use of genomic techniques for supply of drug candidates. Front. Mar. Sci. 5, 401 (2018).Article  Google Scholar  Sweet, M. et al. Insights into the cultured bacterial fraction of corals. mSystems 6, e0124920 (2021).Article  PubMed  PubMed Central  Google Scholar  Pye, C. R., Bertin, M. J., Lokey, R. S., Gerwick, W. H. & Linington, R. G. Retrospective analysis of natural products provides insights for future discovery trends. Proc. Natl Acad. Sci. USA 114, 5601–5606 (2017).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Blin, K. et al. antiSMASH 5.0: Updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res. 47, W81–W87 (2019).Article  PubMed  PubMed Central  CAS  Google Scholar  Pachiadaki, M. G. et al. Charting the complexity of the marine microbiome through single-cell genomics. Cell 179, 1623–1635 (2019).Article  PubMed  PubMed Central  CAS  Google Scholar  Nayfach, S. et al. A genomic catalog of Earth’s microbiomes. Nat. Biotechnol. 39, 499–509 (2021).Article  PubMed  CAS  Google Scholar  Loureiro, C. et al. Comparative metagenomic analysis of biosynthetic diversity across sponge microbiomes highlights metabolic novelty, conservation, and diversification. mSystems 7, e00357-22 (2022).Article  PubMed  PubMed Central  Google Scholar  Paoli, L. et al. Biosynthetic potential of the global ocean microbiome. Nature 607, 111–118 (2022).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  van de Water, J. A., Tignat-Perrier, R., Allemand, D. & Ferrier-Pagès, C. Coral holobionts and biotechnology: from Blue Economy to coral reef conservation. Curr. Opin. Biotechnol. 74, 110–121 (2022).Article  PubMed  Google Scholar  Leopold-Messer, S. et al. Animal-associated marine Acidobacteria with a rich natural-product repertoire. Chem 9, 3696–3713 (2023).Article  CAS  Google Scholar  Voolstra, C. R. et al. Disparate genetic divergence patterns in three corals across a pan-Pacific environmental gradient highlight species-specific adaptation. NPJ Biodivers. 2, 15 (2023).Article  PubMed  PubMed Central  Google Scholar  Lombard, F. et al. Open science resources from the Tara Pacific expedition across coral reef and surface ocean ecosystems. Sci. Data 10, 324 (2023).Article  PubMed  PubMed Central  Google Scholar  Jain, C., Rodriguez-R, L. M., Phillippy, A. M., Konstantinidis, K. T. & Aluru, S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9, 5114 (2018).Article  ADS  PubMed  PubMed Central  Google Scholar  Ruscheweyh, H.-J. et al. Cultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environments. Microbiome 10, 212 (2022).Article  PubMed  PubMed Central  CAS  Google Scholar  Sunagawa, S., Woodley, C. M. & Medina, M. Threatened corals provide underexplored microbial habitats. PLoS ONE 5, e9554 (2010).Article  ADS  PubMed  PubMed Central  Google Scholar  Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).Article  PubMed  Google Scholar  Novichkov, P. S., Wolf, Y. I., Dubchak, I. & Koonin, E. V. Trends in prokaryotic evolution revealed by comparison of closely related bacterial and archaeal genomes. J. Bacteriol. 191, 65–73 (2009).Article  PubMed  CAS  Google Scholar  Giovannoni, S. J., Cameron Thrash, J. & Temperton, B. Implications of streamlining theory for microbial ecology. ISME J. 8, 1553–1565 (2014).Article  PubMed  PubMed Central  Google Scholar  Hentschel, U., Piel, J., Degnan, S. M. & Taylor, M. W. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol. 10, 641–654 (2012).Article  PubMed  CAS  Google Scholar  Voolstra, C. R. et al. The coral microbiome in sickness, in health and in a changing world. Nat. Rev. Microbiol. 22, 460–475 (2024).Article  PubMed  CAS  Google Scholar  Kautsar, S. A., van der Hooft, J. J. J., de Ridder, D. & Medema, M. H. BiG-SLiCE: a highly scalable tool maps the diversity of 1.2 million biosynthetic gene clusters. GigaScience 10, giaa154 (2021).Article  PubMed  PubMed Central  Google Scholar  Ghurye, J. S., Cepeda-Espinoza, V. & Pop, M. Metagenomic assembly: overview, challenges and applications. Yale J. Biol. Med. 89, 353–362 (2016).PubMed  PubMed Central  CAS  Google Scholar  Carroll, A. R., Copp, B. R., Davis, R. A., Keyzers, R. A. & Prinsep, M. R. Marine natural products. Nat. Prod. Rep. 39, 1122–1171 (2022).Article  PubMed  CAS  Google Scholar  Schwarzer, D., Finking, R. & Marahiel, M. A. Nonribosomal peptides: from genes to products. Nat. Prod. Rep. 20, 275–287 (2003).Article  PubMed  CAS  Google Scholar  MarinLit: a Database of the Marine Natural Products Literature (Royal Society of Chemistry, accessed 12 March 2025); https://marinlit.rsc.org/.Burkhardt, I., de Rond, T., Chen, P. Y.-T. & Moore, B. S. Ancient plant-like terpene biosynthesis in corals. Nat. Chem. Biol. 18, 664–669 (2022).Article  PubMed  PubMed Central  CAS  Google Scholar  Crits-Christoph, A., Diamond, S., Butterfield, C. N., Thomas, B. C. & Banfield, J. F. Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis. Nature 558, 440–444 (2018).Article  ADS  PubMed  CAS  Google Scholar  Repka, L. M., Chekan, J. R., Nair, S. K. & van der Donk, W. A. Mechanistic understanding of lanthipeptide biosynthetic enzymes. Chem. Rev. 117, 5457–5520 (2017).Article  PubMed  PubMed Central  CAS  Google Scholar  Zhang, Q., Yu, Y., Vélasquez, J. E. & van der Donk, W. A. Evolution of lanthipeptide synthetases. Proc. Natl Acad. Sci. USA 109, 18361–18366 (2012).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Cavener, D. R. GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J. Mol. Biol. 223, 811–814 (1992).Article  PubMed  CAS  Google Scholar  Sützl, L., Foley, G., Gillam, E. M. J., Bodén, M. & Haltrich, D. The GMC superfamily of oxidoreductases revisited: Analysis and evolution of fungal GMC oxidoreductases. Biotechnol. Biofuels 12, 118 (2019).Article  PubMed  PubMed Central  Google Scholar  Pola, S. in Scope of Selective Heterocycles From Organic and Pharmaceutical Perspective Ch. 1 (ed. Varala, R.) (IntechOpen, 2016).Cox, C. L., Doroghazi, J. R. & Mitchell, D. A. The genomic landscape of ribosomal peptides containing thiazole and oxazole heterocycles. BMC Genomics 16, 778 (2015).Article  PubMed  PubMed Central  Google Scholar  Steinberg, D. A. et al. Protegrin-1: a broad-spectrum, rapidly microbicidal peptide with in vivo activity. Antimicrob. Agents Chemother. 41, 1738–1742 (1997).Article  PubMed  PubMed Central  CAS  Google Scholar  Hoeksema, B. W., Cairns, S. & Samimi-Namin, K. World List of Scleractinia (accessed 20 November 2023); https://www.marinespecies.org/scleractinia.Limborg, M. T., Winther-Have, C. S., Morueta-Holme, N., Gilbert, M. T. P. & Rasmussen, J. A. The overlooked biodiversity loss. Trends Ecol. Evol. 39, 889–891 (2024).Article  PubMed  CAS  Google Scholar  Planes, S. & Allemand, D. Insights and achievements from the Tara Pacific expedition. Nat. Commun. 14, 3131 (2023).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Deshuraud, R. et al. From genome wide SNPs to genomic islands of differentiation: the quest for species diagnostic markers in two scleractinian corals, Pocillopora and Porites. Preprint at bioRxiv https://doi.org/10.1101/2022.10.21.513203 (2022).Pesant, S. et al. Tara Pacific samples provenance and environmental context—version 2. Zenodo https://doi.org/10.5281/ZENODO.4068292 (2020).Belser, C. et al. Integrative omics framework for characterization of coral reef ecosystems from the Tara Pacific expedition. Sci. Data 10, 326 (2023).Article  PubMed  PubMed Central  Google Scholar  Pfeifer, C. R. et al. Quantitative analysis of mouse pancreatic islet architecture by serial block-face SEM. J. Struct. Biol. 189, 44–52 (2015).Article  PubMed  CAS  Google Scholar  Leblud, J., Moulin, L., Batigny, A., Dubois, P. & Grosjean, P. Artificial coral reef mesocosms for ocean acidification investigations. Biogeosci. Discuss. 11, 15463–15505 (2014).ADS  Google Scholar  Meyer, J. L., Gunasekera, S. P., Scott, R. M., Paul, V. J. & Teplitski, M. Microbiome shifts and the inhibition of quorum sensing by Black Band Disease cyanobacteria. ISME J. 10, 1204–1216 (2016).Article  PubMed  CAS  Google Scholar  Cai, L. et al. Metagenomic analysis reveals a green sulfur bacterium as a potential coral symbiont. Sci. Rep. 7, 9320 (2017).Article  ADS  PubMed  PubMed Central  Google Scholar  Sato, Y. et al. Unraveling the microbial processes of black band disease in corals through integrated genomics. Sci. Rep. 7, 40455 (2017).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Wang, L. et al. Corals and their microbiomes are differentially affected by exposure to elevated nutrients and a natural thermal anomaly. Front. Mar. Sci. 5, 101 (2018).Article  CAS  Google Scholar  Robbins, S. J. et al. A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat. Microbiol. 4, 2090–2100 (2019).Article  PubMed  Google Scholar  Yang, S.-H. et al. Metagenomic, phylogenetic, and functional characterization of predominant endolithic green sulfur bacteria in the coral Isopora palifera. Microbiome 7, 3 (2019).Article  PubMed  PubMed Central  Google Scholar  Lima, L. F. O. et al. Modeling of the coral microbiome: the influence of temperature and microbial network. mBio 11, e02691-19 (2020).Article  PubMed  PubMed Central  Google Scholar  Messyasz, A. et al. Coral bleaching phenotypes associated with differential abundances of nucleocytoplasmic large DNA viruses. Front. Mar. Sci. 7, 555474 (2020).Article  Google Scholar  Ngugi, D. K., Ziegler, M., Duarte, C. M. & Voolstra, C. Genomic blueprint of glycine betaine metabolism in coral metaorganisms and their contribution to reef nitrogen budgets. iScience 23, 101120 (2020).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Vohsen, S. A. et al. Deep-sea corals provide new insight into the ecology, evolution, and the role of plastids in widespread apicomplexan symbionts of anthozoans. Microbiome 8, 34 (2020).Article  PubMed  PubMed Central  Google Scholar  Santoro, E. P. et al. Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality. Sci. Adv. 7, eabg3088 (2021).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Keller-Costa, T. et al. Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals. Microbiome 9, 72 (2021).Article  PubMed  PubMed Central  CAS  Google Scholar  Cárdenas, A. et al. Greater functional diversity and redundancy of coral endolithic microbiomes align with lower coral bleaching susceptibility. ISME J. 16, 2406–2420 (2022).Article  PubMed  PubMed Central  Google Scholar  Palladino, G. et al. Metagenomic shifts in mucus, tissue and skeleton of the coral Balanophyllia europaea living along a natural CO2 gradient. ISME Commun. 2, 65 (2022).Article  PubMed  PubMed Central  Google Scholar  Agarwal, V. et al. Metagenomic discovery of polybrominated diphenyl ether biosynthesis by marine sponges. Nat. Chem. Biol. 13, 537–543 (2017).Article  PubMed  PubMed Central  CAS  Google Scholar  Jahn, M. T. et al. A phage protein aids bacterial symbionts in eukaryote immune evasion. Cell Host Microbe 26, 542–550 (2019).Article  PubMed  CAS  Google Scholar  Busch, K. et al. Microbial diversity of the glass sponge Vazella pourtalesii in response to anthropogenic activities. Conserv. Genet. 21, 1001–1010 (2020).Article  CAS  Google Scholar  Engelberts, J. P. et al. Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J. 14, 1100–1110 (2020).Article  PubMed  PubMed Central  CAS  Google Scholar  Glasl, B. et al. Comparative genome-centric analysis reveals seasonal variation in the function of coral reef microbiomes. ISME J. 14, 1435–1450 (2020).Article  PubMed  PubMed Central  Google Scholar  Pascelli, C. et al. Viral ecogenomics across the Porifera. Microbiome 8, 144 (2020).Article  PubMed  PubMed Central  Google Scholar  Storey, M. A. et al. Metagenomic exploration of the marine sponge Mycale hentscheli uncovers multiple polyketide-producing bacterial symbionts. mBio 11, e02997-19 (2020).Article  PubMed  PubMed Central  Google Scholar  Nguyen, N. A. et al. An obligate peptidyl brominase underlies the discovery of highly distributed biosynthetic gene clusters in marine sponge microbiomes. J. Am. Chem. Soc. 143, 10221–10231 (2021).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Rusanova, A., Fedorchuk, V., Toshchakov, S., Dubiley, S. & Sutormin, D. An interplay between viruses and bacteria associated with the white sea sponges revealed by metagenomics. Life (Basel) 12, 25 (2021).ADS  PubMed  PubMed Central  Google Scholar  Robbins, S. J. et al. A genomic view of the microbiome of coral reef demosponges. ISME J. 15, 1641–1654 (2021).Article  PubMed  PubMed Central  CAS  Google Scholar  Dharamshi, J. E. et al. Genomic diversity and biosynthetic capabilities of sponge-associated chlamydiae. ISME J. 16, 2725–2740 (2022).Article  PubMed  PubMed Central  CAS  Google Scholar  Kelly, J. B., Carlson, D. E., Low, J. S. & Thacker, R. W. Novel trends of genome evolution in highly complex tropical sponge microbiomes. Microbiome 10, 164 (2022).Article  PubMed  PubMed Central  CAS  Google Scholar  Morganti, T. M. et al. Giant sponge grounds of Central Arctic seamounts are associated with extinct seep life. Nat. Commun. 13, 638 (2022).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Pankey, M. S. et al. Cophylogeny and convergence shape holobiont evolution in sponge–microbe symbioses. Nat. Ecol. Evol. 6, 750–762 (2022).Article  Google Scholar  Engelberts, J. P. et al. Metabolic reconstruction of the near complete microbiome of the model sponge Ianthella basta. Environ. Microbiol. 25, 646–660 (2023).Article  PubMed  CAS  Google Scholar  Thompson, C. C. et al. Genomic taxonomy of vibrios. BMC Evol. Biol. 9, 258 (2009).Article  PubMed  PubMed Central  Google Scholar  Kimes, N. E. et al. Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J. 6, 835–846 (2012).Article  PubMed  CAS  Google Scholar  Bondarev, V. et al. The genus Pseudovibrio contains metabolically versatile bacteria adapted for symbiosis. Environ. Microbiol. 15, 2095–2113 (2013).Article  PubMed  PubMed Central  CAS  Google Scholar  Ushijima, B. et al. Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome. Appl. Environ. Microbiol. 80, 2102–2109 (2014).Article  ADS  PubMed  PubMed Central  Google Scholar  Asahina, A. Y. & Hadfield, M. G. Draft genome sequence of Pseudoalteromonas luteoviolacea HI1, determined using Roche 454 and PacBio single-molecule real-time hybrid sequencing. Genome Announc. 3, e01590-14 (2015).Article  PubMed  PubMed Central  Google Scholar  Meyer, J. L. et al. Draft genome sequence of Halomonas meridiana R1t3 isolated from the surface microbiota of the Caribbean Elkhorn coral Acropora palmata. Stand. Genomic Sci. 10, 75 (2015).Article  PubMed  PubMed Central  Google Scholar  Ding, J.-Y., Shiu, J.-H., Chen, W.-M., Chiang, Y.-R. & Tang, S.-L. Genomic insight into the host-endosymbiont relationship of Endozoicomonas montiporae CL-33T with its coral host. Front. Microbiol. 7, 251 (2016).Article  PubMed  PubMed Central  Google Scholar  Franco, T., Califano, G., Gonçalves, A. C., Cúcio, C. & Costa, R. Draft genome sequence of Vibrio sp. strain Evh12, a bacterium retrieved from the gorgonian coral Eunicella verrucosa. Genome Announc. 4, e01729-15 (2016).Article  PubMed  PubMed Central  Google Scholar  Keller-Costa, T., Silva, R., Lago-Lestón, A. & Costa, R. Genomic insights into Aquimarina sp. strain EL33, a bacterial symbiont of the gorgonian coral Eunicella labiata. Genome Announc. 4, e00855-16 (2016).Article  PubMed  PubMed Central  Google Scholar  Wan, X., Miller, J. M., Rowley, S. J., Hou, S. & Donachie, S. P. Draft genome sequence of a novel Luteimonas sp. strain from coral mucus, Hawai’i. Genome Announc. 4, e01228-16 (2016).Article  PubMed  PubMed Central  Google Scholar  Henao, J. et al. Genome sequencing of three bacteria associated to black band disease from a Colombian reef-building coral. Genom. Data 11, 73–74 (2017).Article  PubMed  Google Scholar  Braun, D. R. et al. Complete genome sequence of Dietzia sp. strain WMMA184, a marine coral-associated bacterium. Genome Announc. 6, e01582-17 (2018).Article  PubMed  PubMed Central  Google Scholar  Kumari, P., Badhai, J. & Das, S. K. Draft genome sequence of Marinomonas fungiae strain AN44T (JCM 18476 T), isolated from the coral Fungia echinata from the Andaman Sea. Genome Announc. 6, e00112-18 (2018).Article  PubMed  PubMed Central  Google Scholar  Raimundo, I., Silva, S. G., Costa, R. & Keller-Costa, T. Bioactive secondary metabolites from octocoral-associated microbes: new chances for blue growth. Mar. Drugs 16, 485 (2018).Article  PubMed  PubMed Central  CAS  Google Scholar  Rodrigues, G. N., Lago-Lestón, A., Costa, R. & Keller-Costa, T. Draft genome sequence of Labrenzia sp. strain EL143, a coral-associated Alphaproteobacterium with versatile symbiotic living capability and strong halogen degradation potential. Genome Announc. 6, e00132-18 (2018).Article  PubMed  PubMed Central  Google Scholar  Silva, S. G., Lago-Lestón, A., Costa, R. & Keller-Costa, T. Draft genome sequence of Sphingorhabdus sp. strain EL138, a metabolically versatile Alphaproteobacterium isolated from the gorgonian coral Eunicella labiata. Genome Announc. 6, e00142-18 (2018).Article  PubMed  PubMed Central  Google Scholar  Tandon, K., Chiang, P.-W., Chen, W.-M. & Tang, S.-L. Draft genome sequence of Endozoicomonas acroporae strain Acr-14T, isolated from Acropora coral. Genome Announc. 6, e01576-17 (2018).Article  PubMed  PubMed Central  Google Scholar  Deb, S., Badhai, J. & Das, S. K. Draft genome sequences of two Vibrio fortis strains isolated from coral (Fungia sp.) from the Andaman Sea. Microbiol. Resour. Announc. 9, e01225-19 (2020).Article  PubMed  PubMed Central  Google Scholar  Almeida, J. F. et al. Marine sponge and octocoral-associated bacteria show versatile secondary metabolite biosynthesis potential and antimicrobial activities against human pathogens. Mar. Drugs 21, 34 (2022).Article  PubMed  PubMed Central  Google Scholar  Li, J. et al. Cultured bacteria provide insight into the functional potential of the coral-associated microbiome. mSystems 7, e00327-22 (2022).Article  PubMed  PubMed Central  Google Scholar  Shi, S.-B., Cui, L.-Q., Zeng, Q., Long, L.-J. & Tian, X.-P. Nocardioides coralli sp. nov., an actinobacterium isolated from stony coral in the South China Sea. Int. J. Syst. Evol. Microbiol. 72, 005342 (2022).Article  Google Scholar  Nurk, S., Meleshko, D., Korobeynikov, A. & Pevzner, P. A. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 27, 824–834 (2017).Article  PubMed  PubMed Central  CAS  Google Scholar  Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).Article  PubMed  PubMed Central  CAS  Google Scholar  Kang, D. D. et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 7, e7359 (2019).Article  PubMed  PubMed Central  Google Scholar  Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).Article  PubMed  PubMed Central  CAS  Google Scholar  Eren, A. M. et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3, e1319 (2015).Article  PubMed  PubMed Central  Google Scholar  Bowers, R. M. et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat. Biotechnol. 35, 725–731 (2017).Article  PubMed  PubMed Central  CAS  Google Scholar  Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864–2868 (2017).Article  PubMed  PubMed Central  CAS  Google Scholar  Olm, M. R. et al. Consistent metagenome-derived metrics verify and delineate bacterial species boundaries. mSystems 5, e00731-19 (2020).Article  PubMed  PubMed Central  Google Scholar  Chaumeil, P.-A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36, 1925–1927 (2019).Article  PubMed  PubMed Central  Google Scholar  Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).Article  PubMed  CAS  Google Scholar  Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinf. 11, 119 (2010).Article  Google Scholar  Laslett, D. & Canback, B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 32, 11–16 (2004).Article  PubMed  PubMed Central  CAS  Google Scholar  Milanese, A. et al. Microbial abundance, activity and population genomic profiling with mOTUs2. Nat. Commun. 10, 1014 (2019).Article  ADS  PubMed  PubMed Central  Google Scholar  Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).Article  PubMed  CAS  Google Scholar  Salazar, G. et al. Gene expression changes and community turnover differentially shape the global ocean metatranscriptome. Cell 179, 1068–1083 (2019).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: Accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).Article  PubMed  PubMed Central  CAS  Google Scholar  Huerta-Cepas, J. et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol. Biol. Evol. 34, 2115–2122 (2017).Article  PubMed  PubMed Central  CAS  Google Scholar  Huerta-Cepas, J. et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, D309–D314 (2019).Article  PubMed  PubMed Central  CAS  Google Scholar  Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).Article  PubMed  PubMed Central  CAS  Google Scholar  Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).Article  PubMed  CAS  Google Scholar  Tatusova, T. et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 44, 6614–6624 (2016).Article  PubMed  PubMed Central  CAS  Google Scholar  Kautsar, S. A. et al. MIBiG 2.0: a repository for biosynthetic gene clusters of known function. Nucleic Acids Res. 48, D454–D458 (2020).PubMed  PubMed Central  Google Scholar  Gavriilidou, A. et al. Compendium of specialized metabolite biosynthetic diversity encoded in bacterial genomes. Nat. Microbiol. 8, 726–735 (2022).Article  Google Scholar  Navarro-Muñoz, J. C. et al. A computational framework to explore large-scale biosynthetic diversity. Nat. Chem. Biol. 16, 60–68 (2020).Article  PubMed  Google Scholar  Kautsar, S. A., Blin, K., Shaw, S., Weber, T. & Medema, M. H. BiG-FAM: the biosynthetic gene cluster families database. Nucleic Acids Res. 49, D490–D497 (2021).Article  PubMed  PubMed Central  CAS  Google Scholar  Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37, 540–546 (2019).Article  PubMed  CAS  Google Scholar  Ruscheweyh, H.-J. et al. Tara Pacific 16S rRNA data analysis release. Zenodo https://doi.org/10.5281/ZENODO.4073268 (2022).Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Lohans, C. T. & Vederas, J. C. Structural characterization of thioether-bridged bacteriocins. J. Antibiot. 67, 23–30 (2014).Article  CAS  Google Scholar  Bösch, N. M. et al. Landornamides: antiviral ornithine-containing ribosomal peptides discovered through genome mining. Angew. Chem. Int. Ed. 59, 11763–11768 (2020).Article  Google Scholar  Fuchs, S. W. et al. Entianin, a novel subtilin-like lantibiotic from Bacillus subtilis subsp. spizizenii DSM 15029 T with high antimicrobial activity. Appl. Environ. Microbiol. 77, 1698–1707 (2011).Article  ADS  PubMed  PubMed Central  CAS  Google Scholar  Bhushan, R. & Brückner, H. Marfey’s reagent for chiral amino acid analysis: a review. Amino Acids 27, 231–247 (2004).Article  PubMed  CAS  Google Scholar  Conway, J. R., Lex, A. & Gehlenborg, N. UpSetR: An R package for the visualization of intersecting sets and their properties. Bioinformatics 33, 2938–2940 (2017).Article  PubMed  PubMed Central  CAS  Google Scholar  Lex, A., Gehlenborg, N., Strobelt, H., Vuillemot, R. & Pfister, H. UpSet: visualization of intersecting sets. IEEE Trans. Vis. Comput. Graph. 20, 1983–1992 (2014).Article  PubMed  PubMed Central  Google Scholar  Krassowski, M. krassowski/complex-upset: v1.3.5. Zenodo https://doi.org/10.5281/zenodo.3700590 (2020).Wickham, H. in ggplot2: Elegant Graphics for Data Analysis (ed. Wickham, H.) 189–201 (Springer, 2016).Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).Article  PubMed  CAS  Google Scholar  Cheng, J., Karambelkar, B. & Xie Y. leaflet: create interactive web maps with the JavaScript ‘leafletʼ library. https://doi.org/10.32614/CRAN.package.leaflet (v.2.1.2, 2023).Wiederkehr, F. et al. Unusual enzymology and peptide natural products from novel Acidobacteriota spp. associated with reef-building corals. Zenodo https://doi.org/10.5281/ZENODO.14050210 (2024).Paoli, L., Wiederkehr, F., Ruscheweyh, H.-J. & Sunagawa, S. Coral microbiomes as reservoirs of novel genomic and biosynthetic diversity. Zenodo https://doi.org/10.5281/ZENODO.10182966 (2025).Paoli, L. & Wiederkehr, F. SushiLab/reef-microbiomics-paper: initial release for archiving at zenodo. Zenodo https://doi.org/10.5281/zenodo.10201847 (2023).Tara Pacific Consortium. Tara Pacific expedition participants. Zenodo https://doi.org/10.5281/zenodo.3777759 (2020).Apprill, A., Weber, L. G. & Santoro, A. E. Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems 1, e00143-16 (2016).Article  PubMed  PubMed Central  Google Scholar 

View Original Article