Algae dictate multiple stressor effects on coral microbiomes
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.
KeywordsVermetid Algal turf Microbiome Coral–algal interactions Stressors
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.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Allen-Jacobson LM (2018) Life in a colony: growth, morphology, and metabolic scaling. PhD thesis. University of FloridaGoogle Scholar
- Brown AL (2018) Trait mediated effects and the extended phenotype: community interactions on coral reefs. PhD thesis, University of GeorgiaGoogle 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 7:335–336CrossRefGoogle 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:e01035–17–41Google 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. ElsevierGoogle Scholar
- Lenihan HS (1999) Physical-biological coupling on oyster reefs: how habitat structure influences individual performance. Ecol Mon 69(3):251–275Google Scholar
- Martin MO (2002) Predatory prokaryotes: an emerging research opportunity. J Mol Microbiol Biotechnol 4(5):467–478Google 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 962Google 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, HeidelbergGoogle 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. 748Google 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 7:1–12CrossRefGoogle Scholar