Comparative genome-centric analysis reveals seasonal variation in the function of coral reef microbiomes

De’ath G, Fabricius KE, Sweatman H, Puotinen M. The 27-year decline of coral cover on the Great Barrier Reef and its causes. PNAS USA. 2012;109:17995–9.

• Google Scholar

Hoegh-Guldberg O. Coral reefs in the Anthropocene: persistence or the end of the line? Geol Soc Spec Publ. 2014;395:167–83.

• Google Scholar

Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JBC, et al. Coral reefs in the Anthropocene. Nature. 2017;546:82–90.

• Google Scholar

Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, et al. Climate change, human impacts, and the resilience of coral reefs. Science. 2003;301:929–33.

• Google Scholar

Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, et al. Global warming transforms coral reef assemblages. Nature. 2018;556:492–6.

• Google Scholar

Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VG. Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology. 2009;90:1478–84.

• Google Scholar

Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, et al. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol. 2007;17:360–5.

• Google Scholar

Haas AF, Fairoz MFM, Kelly LW, Nelson CE, Dinsdale EA, Edwards RA, et al. Global microbialization of coral reefs. Nat Microbiol. 2016;1:16042.

• Google Scholar

Ainsworth TD, Gates RD. Corals’ microbial sentinels. Science. 2016;352:1518–9.

• Google Scholar

Webster NS, Reusch TBH. Microbial contributions to the persistence of coral reefs. Isme J. 2017;11:2167–74.

• Google Scholar

Bourne DG, Morrow KM, Webster NS. Coral Holobionts: insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol. 2016;70:317–40.

• Google Scholar

McDevitt-Irwin JM, Baum JK, Garren M, Thurber RLV. Responses of coral-associated bacterial communities to local and global stressors. Front Mar Sci. 2017;4:262.

• Google Scholar

Morrow KM, Bourne DG, Humphrey C, Botte ES, Laffy P, Zaneveld J, et al. Natural volcanic CO₂ seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J. 2015;9:894–908.

• Google Scholar

Pita L, Rix L, Slaby BM, Franke A, Hentschel U. The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome. 2018;6:46.

• Google Scholar

Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun. 2017;8:14213.

• Google Scholar

Bourne D, Iida Y, Uthicke S, Smith-Keune C. Changes in coral-associated microbial communities during a bleaching event. ISME J. 2008;2:350–63.

• Google Scholar

Fan L, Liu M, Simister R, Webster NS, Thomas T. Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME J. 2013;7:991–1002.

• Google Scholar

Glasl B, Herndl GJ, Frade PR. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 2016;10:2280–92.

• Google Scholar

Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R, Payet JP, et al. Overfishing and nutrient polution interact with temperature to disrupt coral reefs down to microbial scales. Nat Commun. 2016;7:11833.

• Google Scholar

De Goeij JM, van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, de Goeij AFPM, et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science. 2013;342:108–10.

• Google Scholar

McDole T, Nulton J, Barott KL, Felts B, Hand C, Hatay M, et al. Assessing coral reefs on a pacific-wide scale using the microbialization score. PLoS ONE. 2012;7:e43233.

• Google Scholar

Haas AF, Nelson CE, Kelly LW, Carlson CA, Rohwer F, Leichter JJ, et al. Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity. PLoS ONE. 2011;6:e27973.

• Google Scholar

Morrow KM, Paul VJ, Liles MR, Chadwick NE. Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms. Coral Reefs. 2011;30:309–20.

• Google Scholar

Nelson CE, Goldberg SJ, Kelly LW, Haas AF, Smith JE, Rohwer F, et al. Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J. 2013;7:962–79.

• Google Scholar

Nugues MM, Smith GW, Hooidonk RJ, Seabra MI, Bak RPM. Algal contact as a trigger for coral disease. Ecol Lett. 2004;7:919–23.

• Google Scholar

Sweet MJ, Bythell JC, Nugues MM. Algae as reservoirs for coral pathogens. PLoS ONE. 2013;8:e69717.

• Google Scholar

Vega Thurber R, Burkepile DE, Correa AM, Thurber AR, Shantz AA, Welsh R, et al. Macroalgae decrease growth and alter microbial community structure of the reef-building coral, Porites astreoides. PLoS ONE. 2012;7:e44246.

• Google Scholar

Barott KL, Rohwer FL. Unseen players shape benthic competition on coral reefs. Trends Microbiol. 2012;20:621–8.

• Google Scholar

Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L, et al. Microbial ecology of four coral atolls in the northern Line Islands. PLoS ONE. 2008;3:e1584.

• Google Scholar

Vega Thurber RL, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, et al. Metagenomic analysis of stressed coral holobionts. Environ Microbiol. 2009;11:2148–63.

• Google Scholar

Garren M, Azam F. New directions in coral reef microbial ecology. Environ Microbiol. 2012;14:833–44.

• Google Scholar

Glasl B, Webster NS, Bourne DG. Microbial indicators as a diagnostic tool for assessing water quality and climate stress in coral reef ecosystems. Mar Biol. 2017;164:91.

• Google Scholar

Imelfort M, Parks D, Woodcroft BJ, Dennis P, Hugenholtz P, Tyson GW. GroopM: an automated tool for the recovery of population genomes from related metagenomes. PeerJ. 2014;2:e603.

• Google Scholar

Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165–1165.

• Google Scholar

Wu Y-W, Simmons BA, Singer SW. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics. 2016;32:605–7.

• Google Scholar

Ceccarelli DM, Evans RD, Logan M, Mantel P, Puotinen M, Petus C. et al. Long-term dynamics and drivers of coral and macroalgal cover on inshore reefs of the Great Barrier Reef Marine Park. Ecol Appl. 2019;0:e02008

• Google Scholar

De’ath G, Fabricius K. Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl. 2010;20:840–50.

• Google Scholar

Wismer S, Hoey AS, Bellwood DR. Cross-shelf benthic community structure on the Great Barrier Reef: relationships between macroalgal cover and herbivore biomass. Mar Ecol Prog Ser. 2009;376:45–54.

• Google Scholar

Ceccarelli DM, Loffler Z, Bourne DG, Al Moajil-Cole GS, Boström-Einarsson L, Evans-Illidge E, et al. Rehabilitation of coral reefs through removal of macroalgae: state of knowledge and considerations for management and implementation. Restor Ecol. 2018;26:827–38.

• Google Scholar

Schaffelke B, Klumpp DW. Biomass and productivity of tropical macroalgae on three nearshore fringing reefs in the central Great Barrier Reef, Australia. Bot Mar. 1997;40:373–83.

• Google Scholar

Mellin C, Matthews S, Anthony KRN, Brown SC, Caley MJ, Johns KA, et al. Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts. Glob Change Biol. 2019;25:2431–45.

• Google Scholar

Walther BD, Kingsford MJ, McCulloch MT. Environmental records from Great Barrier Reef corals: inshore versus offshore drivers. PLoS ONE. 2013;8:e77091.

• Google Scholar

Devlin MJ, Lorey MJ. Water quality – field and analyitical procedures. In: Long-term monitoring Great Barrier Reef, editor. Standard Operational Procedues, vol 6. Townsville: Australian Institute of Marine Science; 2000.

Glasl B, Bourne DG, Frade PR, Thomas T, Schaffelke B, Webster NS. Microbial indicators of environmental perturbations in coral reef ecosystems. Microbiome. 2019a;7:94.

• Google Scholar

Botte ES, Nielsen S, Abdul Wahab MA, Webster J, Robbins S, Thomas T, et al. Changes in the metabolic potential of the sponge microbiome under ocean acidification. Nat Commun. 2019;10:4134.

• Google Scholar

Sturm M, Schroeder C, Bauer P. SeqPurge: highly-sensitive adapter trimming for paired-end NGS data. BMC Bioinforma. 2016;17:208.

• Google Scholar

Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.

• Google Scholar

Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.

• Google Scholar

Olm MR, Brown CT, Brooks B, Banfield JF. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. Isme J. 2017;11:2864–8.

• Google Scholar

Krüger K, Chafee M, Ben Francis T, Glavina del Rio T, Becher D, Schweder T, et al. In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes. ISME J. 2019;13:2800–16.

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2019. https://www.R-project.org/.

Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. R package version 2.5-6. 2019. https://CRAN.R-project.org/package=vegan.

Chen H. VennDiagram: generate high-resolution Venn and Euler plots. R package version 1.6.20. 2018. https://CRAN.Rproject.org/package=VennDiagram.

Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106.

• Google Scholar

McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.

• Google Scholar

Wickham H. ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York, 2016.

Clark-Carter, D. z Scores. In Wiley StatsRef: Statistics Reference Online (eds Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL). 2014. https://doi.org/10.1002/9781118445112.stat06236.

Webster NS, Thomas T. The sponge hologenome. mBio. 2016;7:e00135–16.

• Google Scholar

Grondin JM, Tamura K, Déjean G, Abbott DW, Brumer H. Polysaccharide utilization loci: fueling microbial communities. J Bacteriol. 2017;199:e00860–00816.

• Google Scholar

Viborg AH, Terrapon N, Lombard V, Michel G, Czjzek M, Henrissat B, et al. A subfamily roadmap for functional glycogenomics of the evolutionarily diverse glycoside hydrolase family 16 (GH16). J Biol Chem. 2019. https://doi.org/10.1074/jbc.RA119.010619.

Becker S, Scheffel A, Polz MF, Hehemann JH. Accurate quantification of laminarin in marine organic matter with enzymes from marine microbes. Appl Environ Microbiol. 2017;83:e03389–16.

• Google Scholar

Rioux LE, Turgeon SL, Beaulieu M. Characterization of polysaccharides extracted from brown seaweeds. Carbohydr Polym. 2007;69:530–7.

• Google Scholar

Mühlenbruch M, Grossart H-P, Eigemann F, Voss M. Mini-review: phytoplankton-derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria. Environ Microbiol. 2018;20:2671–85.

• Google Scholar

Lerouge I, Vanderleyden J. O‐antigen structural variation: mechanisms and possible roles in animal/plant–microbe interactions. FEMS Microbiol Rev. 2006;26:17–47.

• Google Scholar

Wang X, Quinn PJ, Yan A. Kdo2-lipid A: structural diversity and impact on immunopharmacology. Biol Rev. 2015;90:408–27.

• Google Scholar

Kovacs-Simon A, Titball RW, Michell SL. Lipoproteins of bacterial pathogens. Infect Immun. 2011;79:548–61.

• Google Scholar

Dowhan W, Bogdanov M. Functional roles of lipids in membranes. In: Vance DE, Vance JE, editors. Biochemistry of lipids, lipoproteins and membranes. Amsterdam, The Netherlands: Elsevier Science; 2002.

• Google Scholar

Angly FE, Heath C, Morgan TC, Tonin H, Rich V, Schaffelke B, et al. Marine microbial communities of the Great Barrier Reef lagoon are influenced by riverine floodwaters and seasonal weather events. PeerJ. 2016;4:e1511.

• Google Scholar

Kelly LW, Williams GJ, Barott KL, Carlson CA, Dinsdale EA, Edwards RA, et al. Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. PNAS. 2014;111:10227–32.

• Google Scholar

Lefèvre CD, Bellwood DR. Seasonality and dynamics in coral reef macroalgae: variation in condition and susceptibility to herbivory. Mar Biol. 2010;157:955–65.

• Google Scholar

Zubia M, Payri C, Deslandes E. Alginate, mannitol, phenolic compounds and biological activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria ornata (Phaeophyta: Fucales), from Tahiti (French Polynesia). J Appl Phycol. 2008;20:1033–43.

• Google Scholar

Saier MHJ. The bacterial phosphotransferase system: new frontiers 50 years after its discovery. J Mol Microbiol Biotechnol. 2015;25:73–78.

• Google Scholar

Nakanishi K, Nishijima M, Nishimura M, Kuwano K, Saga N. Bacteria that induce morphogenesis in Ulva pertusa (Chlorophyta) grown under axenic conditions. J Phycol. 1996;32:479–82.

• Google Scholar

Singh RP, Mantri VA, Reddy CRK, Jha B. Isolation of seaweed-associated bacteria and their morphogenesis-inducing capability in axenic cultures of the green alga Ulva fasciata. Aquat Biol. 2011;12:13–21.

• Google Scholar

Singh RP, Reddy CRK. Unraveling the functions of the macroalgal microbiome. Front Microbiol. 2016;6:1488.

• Google Scholar

Glasl B, Smith CE, Bourne DG, Webster NS. Disentangling the effect of host-genotype and environment on the microbiome of the coral Acropora tenuis. PeerJ. 2019b;7:e6377.

• Google Scholar

Diaz MC, Rützler K. Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci. 2001;69:535–46.

• Google Scholar

Webster NS, Taylor MW. Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol. 2012;14:335–46.

• Google Scholar

Moitinho-Silva L, Steinert G, Nielsen S, Hardoim CCP, Wu YC, McCormack GP, et al. Predicting the HMA-LMA status in marine sponges by machine learning. Front Microbiol. 2017;8:752.

• Google Scholar

Burgsdorf I, Slaby BM, Handley KM, Haber M, Blom J, Marshall CW, et al. Lifestyle evolution in cyanobacterial symbionts of sponges. mBio. 2015;6:e00391–00315.

• Google Scholar