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      Oceanographic habitat and the coral microbiomes of urban-impacted reefs

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          Abstract

          Coral reefs are in decline worldwide. In response to this habitat loss, there are efforts to grow, outplant, and restore corals in many regions. The physical oceanographic habitat of corals—such as sea temperature, waves, ocean currents, and available light—is spatially heterogeneous. We therefore hypothesize that outplant location may affect microbiomes, and ultimately, coral health and restoration success. We evaluated the influence of the physical oceanographic habitat on microbes in wild Porites astreoides and Siderastrea siderea. Tissue samples were collected at four Florida reefs in March, June, and September of 2015. We estimated oceanographic conditions from moored instruments, diver observations, remote sensing data, and numerical models. We analyzed microbiomes using amplicon 16S rRNA high-throughput sequencing data. We found microbial alpha-diversity negatively correlated with in situ sea temperature (which represented both the annual cycle and upwelling), as well as modeled alongshore currents, in situ sea-level, and modeled tide. Microbial beta-diversity correlated positively with significant wave height and alongshore currents from models, remotely-sensed relative turbidity, and in situ temperature. We found that archaea from the order Marine Group II decrease with increases in significant wave height, suggesting that this taxon may be influenced by waves. Also, during times of high wave activity, the relative abundance of bacteria from the order Flavobacteriales increases, which may be due to resuspension and cross-shelf transport of sediments. We also found that bacteria from the order SAR86 increase in relative abundance with increased temperature, which suggests that this taxon may play a role in the coral microbiome during periods of higher temperature. Overall, we find that physical oceanographic variability correlates with the structure of these coral microbiomes in ways that could be significant to coral health.

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          Most cited references61

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          Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage

          Bacteria in the 16S rRNA clade SAR86 are among the most abundant uncultivated constituents of microbial assemblages in the surface ocean for which little genomic information is currently available. Bioinformatic techniques were used to assemble two nearly complete genomes from marine metagenomes and single-cell sequencing provided two more partial genomes. Recruitment of metagenomic data shows that these SAR86 genomes substantially increase our knowledge of non-photosynthetic bacteria in the surface ocean. Phylogenomic analyses establish SAR86 as a basal and divergent lineage of γ-proteobacteria, and the individual genomes display a temperature-dependent distribution. Modestly sized at 1.25–1.7 Mbp, the SAR86 genomes lack several pathways for amino-acid and vitamin synthesis as well as sulfate reduction, trends commonly observed in other abundant marine microbes. SAR86 appears to be an aerobic chemoheterotroph with the potential for proteorhodopsin-based ATP generation, though the apparent lack of a retinal biosynthesis pathway may require it to scavenge exogenously-derived pigments to utilize proteorhodopsin. The genomes contain an expanded capacity for the degradation of lipids and carbohydrates acquired using a wealth of tonB-dependent outer membrane receptors. Like the abundant planktonic marine bacterial clade SAR11, SAR86 exhibits metabolic streamlining, but also a distinct carbon compound specialization, possibly avoiding competition.
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            The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance

            Microbes are well-recognized members of the coral holobiont. However, little is known about the short-term dynamics of mucus-associated microbial communities under natural conditions and after disturbances, and how these dynamics relate to the host's health. Here we examined the natural variability of prokaryotic communities (based on 16S ribosomal RNA gene amplicon sequencing) associating with the surface mucus layer (SML) of Porites astreoides, a species exhibiting cyclical mucus aging and shedding. Shifts in the prokaryotic community composition during mucus aging led to the prevalence of opportunistic and potentially pathogenic bacteria (Verrucomicrobiaceae and Vibrionaceae) in aged mucus and to a twofold increase in prokaryotic abundance. After the release of aged mucus sheets, the community reverted to its original state, dominated by Endozoicimonaceae and Oxalobacteraceae. Furthermore, we followed the fate of the coral holobiont upon depletion of its natural mucus microbiome through antibiotics treatment. After re-introduction to the reef, healthy-looking microbe-depleted corals started exhibiting clear signs of bleaching and necrosis. Recovery versus mortality of the P. astreoides holobiont was related to the degree of change in abundance distribution of the mucus microbiome. We conclude that the natural prokaryotic community inhabiting the coral SML contributes to coral health and that cyclical mucus shedding has a key role in coral microbiome dynamics.
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              Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors.

              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.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ Inc. (San Diego, USA )
                2167-8359
                10 September 2019
                2019
                : 7
                : e7552
                Affiliations
                [1 ] Cooperative Institute for Marine and Atmospheric Studies, University of Miami , Miami, FL, USA
                [2 ] Atlantic Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration , Miami, FL, USA
                Author information
                http://orcid.org/0000-0003-4772-1991
                Article
                7552
                10.7717/peerj.7552
                6743471
                31565557
                8cb893df-7152-402b-adde-20315bb7e177
                © 2019 Rosales et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 5 April 2019
                : 25 July 2019
                Funding
                Funded by: NOAA’s Coral Reef Conservation Program (CRCP Project #1114)
                Funded by: NOAA ’Omics Initiative
                The study was funded by NOAA’s Coral Reef Conservation Program (CRCP Project #1114) and by the NOAA ’Omics Initiative. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Marine Biology
                Microbiology
                Biological Oceanography

                currents,bacteria,waves,temperature,archaea,turbidity,tides,oceanography

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