An unusual microbiome characterises a spatially-aggressive crustose alga rapidly overgrowing shallow Caribbean reefs
1.
Jackson, J., Donovan, M., Cramer, K. & Lam, V. Status and Trends of Caribbean Coral Reefs: 1970–2012. Glob. Coral Reef Monit. Network, Int. Union for Conserv. Nat. Glob. Mar. Polar Program, Washington, DC (2014).
2.
Baird, A. H., Babcock, R. C. & Mundy, C. P. Habitat selection by larvae influences the depth distribution of six common coral species. Mar. Ecol. Prog. Ser. 252, 289–293 (2003).
ADS Article Google Scholar
3.
Harrington, L., Fabricius, K., De’ath, G. & Negri, A. Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecol. 85, 3428–3437 (2004).
Article Google Scholar
4.
Roff, G. & Mumby, P. J. Global disparity in the resilience of coral reefs. Trends Ecol. & Evol. 27, 404–413 (2012).
PubMed Article PubMed Central Google Scholar
5.
Lessios, H. A. Mass mortality of Diadema antillarum in the Caribbean: What Have We Learned? Annu. Rev. Ecol. Syst. 19, 371–393 (1988).
Article Google Scholar
6.
Patterson, K. L. et al. The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc. Natl. Acad. Sci. 99, 8725–8730 (2002).
7.
Eakin, C. M. et al. Caribbean Corals in Crisis: Record Thermal Stress, Bleaching, and Mortality in 2005. PLoS ONE 5, 1–9 (2010).
Article CAS Google Scholar
8.
Wilkinson, C. R. In Status of Coral Reefs of the World: 2004 (Townsville: Australian Institute of Marine Science, 2004).
Google Scholar
9.
Miller, J., Waara, R., Muller, E. & Rogers, C. Coral bleaching and disease combine to cause extensive mortality on reefs in US Virgin Islands. Coral Reefs 25, 418 (2006).
Article Google Scholar
10.
Donner, S. D., Knutson, T. R. & Oppenheimer, M. Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc. Natl. Acad. Sci. 104, 5483–5488 (2007).
ADS CAS PubMed Article PubMed Central Google Scholar
11.
Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nat. 543, 373–377 (2017).
ADS CAS PubMed Article PubMed Central Google Scholar
12.
Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A. & Watkinson, A. R. Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecol. 86, 174–184 (2005).
Article Google Scholar
13.
Smith, S. R. Patterns of Coral Recruitment and Post-Settlement Mortality on Bermuda’s Reefs: Comparisons to Caribbean and Pacific Reefs. Am. Zool. 32, 663–673 (1992).
Article Google Scholar
14.
Arnold, S. N. & Steneck, R. S. Settling into an Increasingly Hostile World: The Rapidly Closing “Recruitment Window” for Corals. PLoS ONE 6, e28681 (2011).
ADS CAS PubMed PubMed Central Article Google Scholar
15.
Edmunds, P. J. et al. Geographic variation in long-term trajectories of change in coral recruitment: a global-to-local perspective. Mar. Freshw. Res. 66, 609–622 (2015).
Article Google Scholar
16.
Glassom, D., Zakai, D. & Chadwick-Furman, N. Coral recruitment: a spatio-temporal analysis along the coastline of Eilat, northern Red Sea. Mar. Biol. 144, 641–651 (2004).
Article Google Scholar
17.
Edmunds, P. J. et al. Why more comparative approaches are required in time-series analyses of coral reef ecosystems. Mar. Ecol. Prog. Ser. 608, 297–306 (2019).
ADS Article Google Scholar
18.
Hughes, T. P. Catastrophes, Phase Shifts, and Large-Scale Degradation of a Caribbean Coral Reef. Sci. 265, 1547–1551 (1994).
ADS CAS PubMed Article Google Scholar
19.
Jackson, J. B. C. et al. Historical Overfishing and the Recent Collapse of Coastal Ecosystems. Sci. 293, 629–637 (2001).
CAS PubMed Article PubMed Central Google Scholar
20.
McCook, L. Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367 (1999).
Article Google Scholar
21.
Loh, T., McMurray, S. E., Henkel, T. P., Vicente, J. & Pawlik, J. R. Indirect effects of overfishing on Caribbean reefs: sponges overgrow reef-building corals. PeerJ 3, e901 (2015).
PubMed PubMed Central Article Google Scholar
22.
Lenz, E., Bramanti, L., Lasker, H. & Edmunds, P. J. Long-term variation of octocoral populations in St. John, US Virgin Islands. Coral Reefs 34, 1099–1109 (2015).
ADS Article Google Scholar
23.
Gleason, D. F. & Hofmann, D. K. Coral larvae: From gametes to recruits. J. Exp. Mar. Biol. Ecol. 408, 42–57 (2011).
Article Google Scholar
24.
Siboni, N. et al. Using Bacterial Extract along with Differential Gene Expression in Acropora millepora Larvae to Decouple the Processes of Attachment and Metamorphosis. PLoS ONE 7, e37774 (2012).
ADS CAS PubMed PubMed Central Article Google Scholar
25.
Doropoulos, C. et al. Characterizing the ecological trade-offs throughout the early ontogeny of coral recruitment. Ecol. Monogr. 86, 20–44 (2016).
Google Scholar
26.
Ritson-Williams, R., Arnold, S. N., Paul, V. J. & Steneck, R. S. Larval settlement preferences of Acropora palmata and Montastraea faveolata in response to diverse red algae. Coral Reefs 33, 59–66 (2014).
ADS Article Google Scholar
27.
Ritson-Williams, R., Paul, V. J., Arnold, S. N. & Steneck, R. S. Larval settlement preferences and post-settlement survival of the threatened caribbean corals Acropora palmata and A. cervicornis. Coral Reefs 29, 71–81 (2010).
ADS Article Google Scholar
28.
Johnson, C. R., Muir, D. G. & Reysenbach, A. L. Characteristic bacteria associated with surfaces of coralline algae: a hypothesis for bacterial induction of marine invertebrate larvae. Mar. Ecol. Prog. Ser. 74, 281–294 (1991).
ADS Article Google Scholar
29.
Heyward, A. J. & Negri, A. P. Natural inducers for coral larval metamorphosis. Coral Reefs 18, 273–279 (1999).
Article Google Scholar
30.
Webster, N. S. et al. Metamorphosis of a Scleractinian Coral in Response to Microbial Biofilms. Appl. Environ. Microbiol. 70, 1213–1221 (2004).
CAS PubMed PubMed Central Article Google Scholar
31.
Hadfield, M. G. Biofilms and Marine Invertebrate Larvae: What Bacteria Produce that Larvae Use to Choose Settlement Sites. Annu. Rev. Mar. Sci. 3, 453–470 (2011).
ADS Article Google Scholar
32.
Sneed, J. M., Ritson-Williams, R. & Paul, V. J. Crustose coralline algal species host distinct bacterial assemblages on their surfaces. ISME J. 9, 2527–2536 (2015).
PubMed PubMed Central Article Google Scholar
33.
Negri, A. P., Webster, N. S., Hill, R. T. & Heyward, A. J. Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar. Ecol. Prog. Ser. 223, 121–131 (2001).
ADS Article Google Scholar
34.
Sneed, J. M., Sharp, K. H., Ritchie, K. B. & Paul, V. J. The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals. Proc. Royal Soc. B 281, 20133086 (2014).
PubMed Article CAS PubMed Central Google Scholar
35.
Tebben, J. et al. Induction of Larval Metamorphosis of the Coral Acropora millepora by Tetrabromopyrrole Isolated from a Pseudoalteromonas Bacterium. PLoS ONE 6, e19082 (2011).
ADS CAS PubMed PubMed Central Article Google Scholar
36.
Tebben, J. et al. Chemical mediation of coral larval settlement by crustose coralline algae. Sci. Reports 5, 10803 (2015).
ADS CAS PubMed PubMed Central Article Google Scholar
37.
Morse, D. E., Morse, A. N. C., Raimondi, P. T. & Hooker, N. Morphogen-Based Chemical Flypaper for Agaricia humilis Coral Larvae. The Biol. Bull. 186, 172–181 (1994).
CAS PubMed Article Google Scholar
38.
Raimondi, P. T. & Morse, A. N. C. The consequences of complex larval behavior in a coral. Ecol. 81, 3193–3211 (2000).
Article Google Scholar
39.
Antonius, A. & Ballesteros, E. Epizoism: a new threat to coral health in Caribbean reefs. Revista de Biol. Trop. 46, 145–156 (1998).
Google Scholar
40.
Verlaque, M., Ballesteros, E. & Antonius, A. Metapeyssonnelia corallepida sp. nov. (Peyssonneliaceae, Rhodophyta), an Atlantic Encrusting Red Alga Overgrowing Corals. Bot. Mar. 43, 191–200 (2000).
41.
Pueschel, C. M. & Saunders, G. W. Ramicrusta textilis sp. nov. (Peyssonneliaceae, Rhodophyta), an anatomically complex Caribbean alga that overgrows corals. Phycol. 48, 480–491 (2009).
Article Google Scholar
42.
Eckrich, C. E., Engel, M. S. & Peachey, R. B. J. Crustose, calcareous algal bloom (Ramicrusta sp.) overgrowing scleractinian corals, gorgonians, a hydrocoral, sponges, and other algae in Lac Bay, Bonaire, Dutch Caribbean. Coral Reefs 30, 131–131 (2011)
43.
Eckrich, C. E. & Engel, M. S. Coral overgrowth by an encrusting red alga (Ramicrusta sp.): a threat to Caribbean reefs?. Coral Reefs 32, 81–84 (2013).
44.
Ballantine, D. & Ruiz, H. Metapeyssonnelia milleporoides, a new species of coral-killing red alga (Peyssonneliaceae) from Puerto Rico, Caribbean Sea. Bot. Mar. 54, 47–51 (2011).
45.
Edmunds, P. J., Zimmerman, S. A. & Bramanti, L. A spatially aggressive peyssonnelid algal crust (PAC) threatens shallow coral reefs in St. John, US Virgin Islands. Coral Reefs 38, 1329–1341 (2019).
46.
Basso, D. Carbonate production by calcareous red algae and global change. Geodiversitas 34, 13–33 (2012).
47.
Taylor, W. & Arndt, C. The marine algae of the southwestern Peninsula of Hispaniola. Am. J. Bot. 16, 651–662 (1929).
48.
Van Den Hoek, C., Cortel-Breeman, A. & Wanders, J. Algal zonation in the fringing coral reef of Curaçao, Netherlands Antilles, in relation to zonation of corals and gorgonians. Aquatic. Bot. 1, 269–308 (1975).
49.
Sammarco, P. W. Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. J. Exp. Mar. Biol. Ecol. 65, 83–105 (1982).
50.
Littler, M. M., Taylor, P. R., Littler, D. S., Sims, R. H. & Norris, J. N. Dominant macrophyte standing stocks, productivity and community structure on a Belizean barrier-reef. Atoll Res. Bull. 302, 1–24 (1987).
51.
Ballantine, D. & Ruiz, H. A unique red algal reef formation in Puerto Rico. Coral Reefs 32, 411–411 (2013).
52.
Ballantine, D., Ruiz, H., Lozada-Troche, C. & Norris, J. N. The genus Ramicrusta (Peyssonneliales, Rhodophyta) in the Caribbean Sea, including Ramicrusta bonairensis sp. nov. and Ramicrusta monensis sp. nov. Bot. Mar. 59, 417–431 (2016).
53.
Zhang, D. & Zhou, J. Ramicrusta, a new genus of Peyssonneliaceae (Cryptonemiales, Rhodophyta). Oceanol. et Limnol. Sinica 12, 538–544 (1981).
54.
Bramanti, L., Lasker, H. R. & Edmunds, P. J. An encrusting peyssonnellid preempts vacant space and overgrows corals in St. John, US Virgin Islands. Reef Encount. 32, 68–70 (2017).
55.
Tran, C. & Hadfield, M. G. Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria. Mar. Ecol. Prog. Ser. 433, 85–96 (2011).
56.
Golbuu, Y. & Richmond, R. H. Substratum preferences in planula larvae of two species of scleractinian corals, Goniastrea retiformis and Stylaraea punctata. Mar. Biol. 152, 639–644 (2007).
57.
Longford, S. R. et al. Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquatic. Microb. Ecol. 48, 217–229 (2007).
58.
Shade, A. & Handelsman, J. Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol. 14, 4–12 (2011).
59.
Edmunds, P. J. The hidden dynamics of low coral cover communities. Hydrobiol. 818, 193–209 (2018).
60.
Green, D. H., Edmunds, P. J., Pochon, X. & Gates, R. D. The effects of substratum type on the growth, mortality, and photophysiology of juvenile corals in St. John, US Virgin Islands. J. Exp. Mar. Biol. Ecol. 384, 18–29 (2010).
61.
Holmström, C. & Kjelleberg, S. Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol. Ecol. 30, 285–293 (1999).
62.
Offret, C. et al. Spotlight on Antimicrobial Metabolites from the Marine Bacteria Pseudoalteromonas: Chemodiversity and Ecological Significance. Mar. Drugs 14, 129 (2016).
63.
Huang, Y.-L., Dobretsov, S., Xiong, H. & Qian, P.-Y. Effect of Biofilm Formation by Pseudoalteromonas spongiae on Induction of Larval Settlement of the Polychaete Hydroides elegans. Appl. Environ. Microbiol. 73, 6284–6288 (2007).
64.
Wolfaardt, G. M., Lawrence, J. R. & Korber, D. R. Function of EPS. In Wingender, J., Neu, T. R. & Flemming, H. (eds.) Microbial extracellular polymeric substances: characterization, structure, and function, 186–190 (Springer, New York, NY, 1999).
Google Scholar
65.
Huggett, M. J., Williamson, J. E., de Nys, R., Kjelleberg, S. & Steinberg, P. D. Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149, 604–619 (2006).
ADS PubMed Article Google Scholar
66.
Shikuma, N. J., Antoshechkin, I., Medeiros, J. M., Pilhofer, M. & Newman, D. K. Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling. Proc. Natl. Acad. Sci. 113, 10097–10102 (2016).
CAS PubMed Article Google Scholar
67.
Freckleton, M. L., Nedved, B. T. & Hadfield, M. G. Induction of Invertebrate Larval Settlement; Different Bacteria, Different Mechanisms? Sci. Reports 7, 42557 (2017).
68.
Kato, A., Baba, M., Kawai, H. & Masuda, M. Reassessment of the little-known crustose red algal genus Polystrata (Gigartinales), based on morphology and SSU rDNA sequences. J. Phycol. 42, 922–933 (2006).
69.
Dixon, K. R. & Saunders, G. W. DNA barcoding and phylogenetics of Ramicrusta and Incendia gen. nov., two early diverging lineages of the Peyssonneliaceae (Rhodophyta). Phycol. 52, 82–108 (2013).
70.
Nieder, C., Chen, P.-C., Chen, C. A. & Liu, S.-L. New record of the encrusting alga Ramicrusta textilis overgrowing corals in the lagoon of Dongsha Atoll, South China Sea. Bull. Mar. Sci. 95, 459–462 (2019).
71.
Smith, T. B., Ennis, R., Kadison, E., Nemeth, R. S. & Henderson, L. The United States Virgin Islands Territorial Coral Reef Monitoring Program. 2016 Annu. Report, Univ. Virgin Islands, United States Virgin Islands 1–286 (2016).
72.
Adey, W. H. A survey of red algal biology and ecology with reference to carbonate geology, and the role of reds in algal ridge and reef construction. In Recent Advances in Carbonate Studies, vol. 6, 3–6 (West Indies Laboratory, St. Croix, USVI, 1974).
73.
Woelkerling, W. J. South Florida benthic marine algae. In Sedimenta V (University of Miami, 1976).
74.
Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Sci. 318, 1737–1742 (2007).
75.
Hay, M. E. Marine Chemical Ecology: Chemical Signals and Cues Structure Marine Populations, Communities, and Ecosystems. Annu. Rev. Mar. Sci. 1, 193–212 (2009).
76.
Schupp, P. J. & Paul, V. J. Calcium Carbonate and Secondary Metabolites in Tropical Seaweeds: Variable Effects on Herbivorous Fishes. Ecol. 75, 1172–1185 (1994).
77.
Pennings, S. C., Puglisi, M. P., Pitlik, T. J., Himaya, A. C. & Paul, V. J. Effects of secondary metabolites and CaCO(_{3}) on feeding by surgeonfishes and parrotfishes: within-plant comparisons. Mar. Ecol. Prog. Ser. 134, 49–58 (1996).
78.
Blunt, J. W. et al. Marine natural products. Nat. Prod. Reports 24, 31–86 (2007).
79.
Blunt, J. W. et al. Marine natural products. Nat. Prod. Reports 25, 35–94 (2008).
80.
Lane, A. L. et al. Ecological leads for natural product discovery: novel sesquiterpene hydroquinones from the red macroalga Peyssonnelia sp. Tetrahedron 66, 455–461 (2010).
81.
Sawabe, T. et al. Pseudoalteromonas bacteriolytica sp. nov., a marine bacterium that is the causative agent of red spot disease of Laminaria japonica. Int. J. Syst. Evol. Microbiol. 48, 769–774 (1998).
82.
Steneck, R. & Dethier, M. A Functional Group Approach to the Structure of Algal-Dominated Communities. Oikos 69, 476–498 (1994).
83.
Edmunds, P. J. Decadal-scale changes in the community structure of coral reefs of St. John, US Virgin Islands. Mar. Ecol. Prog. Ser. 489, 107–123 (2013).
84.
Wilson, B. et al. Changes in Marine Prokaryote Composition with Season and Depth Over an Arctic Polar Year. Front. Mar. Sci. 4, 95 (2017).
85.
Øvreås, L., Forney, L., Daae, F. L. & Torsvik, V. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol. 63, 3367–3373 (1997).
86.
Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108, 4516–4522 (2011).
87.
Freshwater, D., Fredericq, S. & Bailey, J. Characteristics and utility of nuclear-encoded large-subunit ribosomal gene sequences in phylogenetic studies of red algae. Phycol. Res. 47, 33–38 (1999).
88.
Krayesky, D. M., Norris, J. N., Gabrielson, P. W., Gabriel, D. & Fredericq, S. A new order of red algae based on the Peyssonneliaceae, with an evaluation of the ordinal classification of the Florideophyceae (Rhodophyta). Proc. Biol. Soc. Wash. 122, 364–391 (2009).
89.
Yoon, H. S., Hackett, J. D. & Bhattacharya, D. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. 99, 11724–11729 (2002).
90.
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–6 (2010).
91.
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinforma. 26, 2460–2461 (2010).
92.
Haas, B. J. et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21, 494–504 (2011).
93.
Caporaso, J. G. et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinforma. 26, 266–267 (2009).
94.
DeSantis, T. Z. et al. Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072 (2006).
95.
Joshi, N. A. & Fass, J. N. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33) (2011). Available at https://github.com/najoshi/sickle. Accessed 6 Nov 2020.
96.
Rice, P., Longden, I. & Bleasby, A. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16, 276–277 (2000).
97.
Altschul, S., Gish, W., Miller, W., Myers, E. & Lipman, D. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
98.
GNU General Public License. URL http://www.gnu.org/licenses/gpl.html. Accessed 6 Nov 2020. More