title: Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors.
abstract: Holobionts are species-specific associations between macro- and microorganisms. On coral reefs, the benthic coverage of coral and algal holobionts varies due to natural and anthropogenic forcings. Different benthic macroorganisms are predicted to have specific microbiomes. In contrast, local environmental factors are predicted to select for specific metabolic pathways in microbes. To reconcile these two predictions, we hypothesized that adaptation of microbiomes to local conditions is facilitated by the horizontal transfer of genes responsible for specific metabolic capabilities. To test this hypothesis, microbial metagenomes were sequenced from 22 coral reefs at 11 Line Islands in the central Pacific that together span a wide range of biogeochemical and anthropogenic influences. Consistent with our hypothesis, the percent cover of major benthic functional groups significantly correlated with particular microbial taxa. Reefs with higher coral cover had a coral microbiome with higher abundances of Alphaproteobacteria (such as Rhodobacterales and Sphingomonadales), whereas microbiomes of algae-dominated reefs had higher abundances of Gammaproteobacteria (such as Alteromonadales, Pseudomonadales, and Vibrionales), Betaproteobacteria, and Bacteriodetes. In contrast to taxa, geography was the strongest predictor of microbial community metabolism. Microbial communities on reefs with higher nutrient availability (e.g., equatorial upwelling zones) were enriched in genes involved in nutrient-related metabolisms (e.g., nitrate and nitrite ammonification, Ton/Tol transport, etc.). On reefs further from the equator, microbes had more genes encoding chlorophyll biosynthesis and photosystems I/II. These results support the hypothesis that core microbiomes are determined by holobiont macroorganisms, and that those core taxa adapt to local conditions by selecting for advantageous metabolic genes.
authors: Department of Biology, San Diego State University, San Diego, CA 92182; lwegley@gmail.com.
authors: Linda W
authors: LW
authors: Kelly
authors: Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093;
authors: Gareth J
authors: GJ
authors: Williams
authors: Department of Biology, San Diego State University, San Diego, CA 92182;Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093;
authors: Katie L
authors: KL
authors: Barott
authors: Marine Science Institute, Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106;
authors: Craig A
authors: CA
authors: Carlson
authors: Department of Biology, San Diego State University, San Diego, CA 92182;
authors: Elizabeth A
authors: EA
authors: Dinsdale
authors: Department of Computer Sciences, San Diego State University, San Diego, CA;
authors: Robert A
authors: RA
authors: Edwards
authors: Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093;
authors: Andreas F
authors: AF
authors: Haas
authors: Department of Biology, San Diego State University, San Diego, CA 92182;
authors: Matthew
authors: M
authors: Haynes
authors: Department of Biology, San Diego State University, San Diego, CA 92182;
authors: Yan Wei
authors: YW
authors: Lim
authors: Department of Biology, San Diego State University, San Diego, CA 92182;
authors: Tracey
authors: T
authors: McDole
authors: Center for Microbial Oceanography: Research and Education, Department of Oceanography, University of Hawai'i, Honolulu, HI 96822;
authors: Craig E
authors: CE
authors: Nelson
authors: National Geographic Society, Washington, DC 20036;
authors: Enric
authors: E
authors: Sala
authors: Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093;
authors: Stuart A
authors: SA
authors: Sandin
authors: Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093;
authors: Jennifer E
authors: JE
authors: Smith
authors: Caribbean Research and Management of Biodiversity, Willemstad, Curacao;Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE, Amsterdam, The Netherlands; and.
authors: Mark J A
authors: MJ
authors: Vermeij
authors: Rainbow Rock, Ocean View, HI 96737.
authors: Merry
authors: M
authors: Youle
authors: Department of Biology, San Diego State University, San Diego, CA 92182;
authors: Forest
authors: F
authors: Rohwer
mesh_terms: D000222:Adaptation, Physiological; D001419:Bacteria / Q000235:genetics / Q000378:metabolism; D057894:Coral Reefs; D022761:Gene Transfer, Horizontal; D054892:Metagenome; D064307:Microbiota; D010140:Pacific Ocean; D014876:Water Pollution
keywords: marine bacteria; metabolic potential; microbial biogeography