Skip to main content
Log in

Algae dictate multiple stressor effects on coral microbiomes

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Most studies of stressors focus on the response of traditionally classified organisms via effects on growth, mortality or physiology; however, most species have microbial associates that may mediate the response of a host to the stressor. Additionally, species rarely experience one stressor alone, but instead are influenced by multiple, potentially interacting stressors. We evaluated how coral microbiomes responded to two biotic stressors: the vermetid gastropod, Ceraesignum maximum, and algal turfs, both of which have previously been shown to decrease coral growth, survival and photophysiology. We collected coral mucus from massive Porites colonies in the presence versus absence of both algae and vermetids and sequenced the 16S rRNA gene to characterize the coral surface microbial communities. The presence of algae increased the alpha diversity of the coral microbial community, likely by increasing the relative abundance of rare members of the community. Algae also reduced beta diversity, which we hypothesized was due to algae homogenizing the physical environment. In contrast, vermetids had only small effects on microbial communities, even though vermetids have deleterious effects on coral growth. We previously hypothesized that vermetids would exacerbate algal effects on microbes, but we failed to detect an interaction between vermetids and algae on the coral’s microbiome, except for one family, Fusobacteriaceae, which was most abundant in the presence of both stressors. We suggest that algae can affect corals through their effects on microbes, whereas vermetids primarily affect the host directly; these complementary effects may limit the extent to which stressors can interact.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Allen-Jacobson LM (2018) Life in a colony: growth, morphology, and metabolic scaling. PhD thesis. University of Florida

  • Anderson MJ, Walsh DC (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 4:557–574

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • Barott K, Janouškovec J, Marhaver K, Smith J, Keeling P, Rohwer F (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environmental Microbiology 13:1192–1204

    Article  CAS  PubMed  Google Scholar 

  • Barott KL, Rodriguez-Mueller B, Youle M, Marhaver KL, Vermeij MJA, Smith JE, Rohwer FL (2012) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Proc Biol Sci 279:1655–1664

    Article  PubMed  Google Scholar 

  • Boone MD, Semlitsch RD, Little EE, Doyle MC (2007) Multiple stressors in amphibian communities: effects of chemical contamination, bullfrogs, and fish. Ecol Appl 17:291–301

    Article  PubMed  Google Scholar 

  • Boström KH, Simu K, Hagstrom A, Riemann L (2004) Optimization of DNA extraction for quantitative marine bacterioplankton community analysis. Limnol Oceanogr Methods 2:365–373

    Article  Google Scholar 

  • Bourne DG, Dennis PG, Uthicke S, Soo RM, Tyson GW, Webster N (2013) Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J 7:1452–1458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown AL, Carpenter RC (2013) Water-flow mediated oxygen dynamics within massive Porites-algal turf interactions. Mar Ecol Prog Ser 490:1–10

    Article  CAS  Google Scholar 

  • Brown AL, Carpenter RC (2015) Water flow influences the mechanisms and outcomes of interactions between massive Porites and coral reef algae. Marine Biology 162:459–468

    Article  CAS  Google Scholar 

  • Brown AL, Frazer TK, Shima JS, Osenberg CW (2016) Mass mortality of the vermetid gastropod Ceraesignum maximum. Coral Reefs 35(3):1027–1032

    Article  Google Scholar 

  • Brown AL, Osenberg CW (2018) Vermetid gastropods modify physical and chemical conditions above coral–algal interactions. Oecologia 186:1091–1099. https://doi.org/10.1007/s00442-018-4091-9

    Article  CAS  PubMed  Google Scholar 

  • Brown AL (2018) Trait mediated effects and the extended phenotype: community interactions on coral reefs. PhD thesis, University of Georgia

  • Buck JC, Scheessele EA, Relyea RA, Blaustein AR (2011) The effects of multiple stressors on wetland communities: pesticides, pathogens and competing amphibians. Freshw Biol 57:61–73

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7:335–336

    Article  CAS  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522

    Article  PubMed  Google Scholar 

  • Carpenter R, Williams S (1993) Effects of algal turf canopy height and microscale substratum topography on profiles of flow speed in a coral forereef environment. Limnol and Oceanogr 38:687–694

    Article  Google Scholar 

  • Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315

    Article  PubMed  Google Scholar 

  • Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286

    Article  PubMed  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell Biology of Cnidarian-Dinoflagellate Symbiosis. Microbiol and Mol Biol Rev 76:229–261

    Article  CAS  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Forsman Z, Wellington GM, Fox GE, Toonen RJ (2015) Clues to unraveling the coral species problem: distinguishing species from geographic variation in Porites across the Pacific with molecular markers and microskeletal traits. PeerJ 3:e751–e821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forsman ZH, Barshis DJ, Hunter CL, Toonen RJ (2009) Shape-shifting corals: Molecular markers show morphology is evolutionarily plastic in Porites. BMC Evol Biol 9:45–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas AF, Gregg AK, Smith JE, Abieri ML, Hatay M, Rohwer F (2013a) Visualization of oxygen distribution patterns caused by coral and algae. PeerJ 1:e106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas AF, Nelson CE, Rohwer F, Wegley Kelly L, Quistad SD, Carlson CA, Leichter JJ, Hatay M, Smith JE (2013b) Influence of coral and algal exudates on microbially mediated reef metabolism. PeerJ 1:e108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas AF, Nelson CE, Wegley Kelly L, Carlson CA, Rohwer F, Leichter JJ, Wyatt A, Smith JE (2011) Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity. PLoS ONE 6:e27973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harborne AR, Rogers A, Bozec Y-M, Mumby PJ (2017) Multiple stressors and the functioning of coral reefs. Ann Rev Mar Sci 9:445–468

    Article  PubMed  Google Scholar 

  • Harris JL, Lewis LS, Smith JE (2015) Quantifying scales of spatial variability in algal turf assemblages on coral reefs. Mar Ecol Prog Ser 532:41–57

    Article  Google Scholar 

  • Jompa J, McCook L (2003) Contrasting effects of turf algae on corals: massive Porites spp. are unaffected by mixed-species turfs, but killed by the red alga Anotrichium tenue. Mar Ecol Prog Ser 258:79–86

    Article  Google Scholar 

  • Jorissen H, Skinner C, Osinga R, De Beer D, Nugues MM (2016) Evidence for water-mediated mechanisms in coral–algal interactions. Proc R Soc B 283:20161137

    Article  PubMed  PubMed Central  Google Scholar 

  • Kemp KM, Westrich JR, Alabady MS, Edwards ML, Lipp EK (2018) Abundance and multilocus sequence analysis of Vibriobacteria associated with diseased elkhorn coral (Acropora palmata) of the Florida Keys. J Appl Environ Microbiol 84:e01035–17–41

  • Kline D, Kuntz N, Breitbart M, Knowlton N, Rohwer F (2006) Role of elevated organic carbon levels and microbial activity in coral mortality. Mar Ecol Prog Ser 314:119–125

    Article  CAS  Google Scholar 

  • Klöppel A, Brümmer F, Schwabe D, Morlock G (2013) Detection of bioactive compounds in the mucus nets of Dendropoma maxima, Sowerby 1825 (Prosobranch Gastropod Vermetidae, Mollusca). J Mar Biol 2013:1–10

    Article  Google Scholar 

  • Kuffner I, Walters L, Becerro M, Paul V, Ritson-Williams R, Beach K (2006) Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar Ecol Prog Ser 323:107–117

    Article  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-33. https://CRAN.R-project.org/package=lmerTest

  • Legendre P, Legendre LF (1998) Numerical ecology, 2nd edn. Elsevier

  • Lenihan HS (1999) Physical-biological coupling on oyster reefs: how habitat structure influences individual performance. Ecol Mon 69(3):251–275

    Google Scholar 

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

    Article  Google Scholar 

  • McDonald D, Vázquez-Baeza Y, Walters WA, Caporaso JG, Knight R (2013) From molecules to dynamic biological communities. Biol Philos 28:241–259

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin MO (2002) Predatory prokaryotes: an emerging research opportunity. J Mol Microbiol Biotechnol 4(5):467–478

    CAS  PubMed  Google Scholar 

  • Mera H, Bourne DG (2017) Disentangling causation: complex roles of coral-associated microorganisms in disease. Environmental Microbiology 20:431–449

    Article  PubMed  Google Scholar 

  • Meyer JL, Paul VJ, Teplitski M (2014) Community shifts in the surface microbiomes of the coral Porites astreoides with unusual lesions. PLoS One 9:e100316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mindell DP (1992) Phylogenetic consequences of symbioses: Eukarya and Eubacteria are not monophyletic taxa. BioSystems 27:53–62

    Article  CAS  PubMed  Google Scholar 

  • Morrow KM, Moss AG, Chadwick NE, Liles MR (2012) Bacterial associates of two caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol 78:6438–6449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neave MJ, Apprill A, Ferrier-Pagès C, Voolstra CR (2016) Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl Microbiol Biotechnol 100(19):8315–8324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson CE, Goldberg SJ, Kelly LW, Haas AF, Smith JE, Rohwer F, Carlson CA (2013) Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J 962

  • Nugues MM, Smith GW, Hooidonk RJ, Seabra MI, Bak RP (2004) Algal contact as a trigger for coral disease. Ecol Lett 7:919–923

    Article  Google Scholar 

  • Peixoto RS, Rosado PM, de Leite DCA, Rosado AS, Bourne DG (2017) Beneficial microorganisms for corals (BMC): Proposed mechanisms for coral health and resilience. Front Microbiol 8:100–116

    Article  Google Scholar 

  • Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips NE, Shima JS, Osenberg CW (2014) Live coral cover may provide resilience to damage from the vermetid gastropod Dendropoma maximum by preventing larval settlement. Coral Reefs 33:1137–1144

    Article  Google Scholar 

  • Pratte ZA, Longo GO, Burns AS, Hay ME, Stewart FJ (2017) Contact with turf algae alters the coral microbiome: contact versus systemic impacts. Coral Reefs 37:1–13

    Article  Google Scholar 

  • Rasher D, Hay M (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proceedings of the National Academy of Sciences 107:9683–9688

    Article  Google Scholar 

  • Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc Natl Acad Sci USA 98:2491–2496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environmental Microbiology 8:2068–2073

    Article  CAS  PubMed  Google Scholar 

  • Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91

    Article  Google Scholar 

  • Rudi K, Kroken M, Dahlberg OJ, Deggerdal A, Jakobsen KS, Larsen F (1997) Rapid, universal method to isolate PCR-ready DNA using magnetic beads. BioTechniques 22:506–511

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHM, Szoecs E, Wagner H (2017). vegan: Community Ecology Package. R package version 2.4-5. https://CRAN.R-project.org/package=vegan

  • Olsen I (2014) The Family Fusobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, Heidelberg

    Google Scholar 

  • Shima J, Osenberg C, Stier A (2010) The vermetid gastropod Dendropoma maximum reduces coral growth and survival. Biol Lett 6:815

    Article  PubMed  PubMed Central  Google Scholar 

  • Shaver EC, Shantz AA, McMinds R, Burkepile DE, Vega Thurber RL, Silliman BR (2017) Effects of predation and nutrient enrichment on the success and microbiome of a foundational coral. Ecology 98(3):830–839

    Article  PubMed  Google Scholar 

  • Shima JS, McNaughtan D, Strong AT (2015) Vermetid gastropods mediate within-colony variation in coral growth to reduce rugosity. Marine Biology 162:1523–1530

    Article  CAS  Google Scholar 

  • Shima JS, Phillips NE, Osenberg CW (2013) Consistent deleterious effects of vermetid gastropods on coral performance. J Exp Mar Bio Ecol 439:1–6

    Article  Google Scholar 

  • Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiology Ecology 67(3):371–380

    Article  CAS  PubMed  Google Scholar 

  • Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol Lett 9:835–845

    Article  PubMed  Google Scholar 

  • Staley JT, Whitman WB (2010) Bergey’s Manual of Systematic Bacteriology: Family I. Fusobacteriaceae fam. nov. The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes, p. 748

  • Steneck R, Dethier M (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sweet MJ, Croquer A, Bythell JC (2010) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30(1):39–52

    Article  Google Scholar 

  • Tilman D, Isbell F, Cowles JM (2014) Biodiversity and ecosystem functioning. Annu Rev Ecol Evol Syst 45:471–493

    Article  Google Scholar 

  • Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1(6):6ra14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vega Thurber R, Burkepile DE, Correa AMS, Thurber AR, Shantz AA, Welsh R, Pritchard C, Rosales S (2012) Macroalgae decrease growth and alter microbial community structure of the reef-building coral. Porites astreoides. PLoS ONE 7:e44246

    Article  CAS  PubMed  Google Scholar 

  • Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environmental Microbiology 11:2148–2163

    Article  CAS  PubMed  Google Scholar 

  • Vezzulli L, Previati M, Pruzzo C, Marchese A, Bourne DG, Cerrano C, the VibrioSea Consortium (2010) Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. Environmental Microbiology 12:2007–2019

    Article  CAS  Google Scholar 

  • Wahl M, Goecke F, Labes A, Dobretsov S, Weinberger F (2012) The second skin: ecological role of epibiotic biofilms on marine organisms. Front Microbiol 3:1–21

    Article  CAS  Google Scholar 

  • Wangpraseurt D, Weber M, Røy H, Polerecky L, De Beer D, Suharsono Nugues MM (2012) In situ oxygen dynamics in coral-algal interactions. PLoS ONE 7:e31192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster NS, Negri AP, Botté ES, Laffy PW, Flores F, Noonan S, Schmidt C, Uthicke S (2016) Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. Rep. 6:19324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werner JJ, Koren O, Hugenholtz P, DeSantis TZ, Walters WA, Caporaso JG, Angenent LT, Knight R, Ley RE (2012) Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys. ISME J 6:94-103

    Article  CAS  PubMed  Google Scholar 

  • Zaneveld JR, McMinds R, Thurber RV (2017) Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol 2:1–8

    Article  CAS  Google Scholar 

  • Zaneveld JR, Shantz AA, Pritchard CE, McMinds R, Payet JEROMP, Welsh R, Correa AMS, Lemoine NP, Rosales S, Fuchs C, Maynard JA, Burkepile DE, Thurber RV (2016) Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Comm 7:1–12

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Thanks to M. Teplitski for assistance with sampling protocol, N. Hackney for field assistance, K. Kemp for advice and guidance with DNA protocols, T. Glenn, T. Kieran, J.Thomas for assistance with DNA extraction, and the staff at the Gump Station for assistance with logistics. We also thank the MBL STAMPS 2015 workshop for sharing insights about microbial analyses, and the NSF (OCE-1130359) and the University of Georgia for funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. L. Brown.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Morgan S. Pratchett

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 5303 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brown, A.L., Lipp, E.K. & Osenberg, C.W. Algae dictate multiple stressor effects on coral microbiomes. Coral Reefs 38, 229–240 (2019). https://doi.org/10.1007/s00338-019-01769-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-019-01769-w

Keywords

Navigation