Bacterial Community Associated with the Reef Coral Mussismilia braziliensis's Momentum Boundary Layer over a Diel Cycle

Corals display circadian physiological cycles, changing from autotrophy during the day to heterotrophy during the night. Such physiological transition offers distinct environments to the microbial community associated with corals: an oxygen-rich environment during daylight hours and an oxygen-depleted environment during the night. Most studies of coral reef microbes have been performed on samples taken during the day, representing a bias in the understanding of the composition and function of these communities. We hypothesized that coral circadian physiology alters the composition and function of microbial communities in reef boundary layers. Here, we analyzed microbial communities associated with the momentum boundary layer (MBL) of the Brazilian endemic reef coral Mussismilia braziliensis during a diurnal cycle, and compared them to the water column. We determined microbial abundance and nutrient concentration in samples taken within a few centimeters of the coral's surface every 6 h for 48 h, and sequenced microbial metagenomes from a subset of the samples. We found that dominant taxa and functions in the coral MBL community were stable over the time scale of our sampling, with no significant shifts between night and day samples. Interestingly, the two water column metagenomes sampled 1 m above the corals were also very similar to the MBL metagenomes. When all samples were analyzed together, nutrient concentration significantly explained 40% of the taxonomic dissimilarity among dominant genera in the community. Functional profiles were highly homogenous and not significantly predicted by any environmental variables measured. Our data indicated that water flow may overrule the effects of coral physiology in the MBL bacterial community, at the scale of centimeters, and suggested that sampling resolution at the scale of millimeters may be necessary to address diurnal variation in community composition.

[1]  I. Singleton,et al.  Evidence for rapid, tide-related shifts in the microbiome of the coral Coelastrea aspera , 2017, Coral Reefs.

[2]  M. Bulling,et al.  On the Importance of the Microbiome and Pathobiome in Coral Health and Disease , 2017, Front. Mar. Sci..

[3]  P. Bongaerts,et al.  Microbiome variation in corals with distinct depth distribution ranges across a shallow–mesophotic gradient (15–85 m) , 2017, Coral Reefs.

[4]  M. Sweet,et al.  Coral responses to anthropogenic stress in the 21st century - an ecophsyiological perspective , 2016 .

[5]  M. Brown,et al.  Coral Responses to Anthropogenic Stress in the Twenty- First Century: An Ecophysiological Perspective , 2016 .

[6]  D. Bourne,et al.  Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems. , 2016, Annual review of microbiology.

[7]  C. Voolstra,et al.  Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas , 2016, Applied Microbiology and Biotechnology.

[8]  P. Bongaerts,et al.  The Microbial Signature Provides Insight into the Mechanistic Basis of Coral Success across Reef Habitats , 2016, mBio.

[9]  R. Gates,et al.  Corals' microbial sentinels , 2016, Science.

[10]  Jesse R. Zaneveld,et al.  Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales , 2016, Nature Communications.

[11]  B. Willis,et al.  Implications of Ocean Acidification for Marine Microorganisms from the Free-Living to the Host-Associated , 2016, Front. Mar. Sci..

[12]  John H. Werren,et al.  Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts , 2016, mBio.

[13]  Barbara A. Bailey,et al.  Lytic to temperate switching of viral communities , 2016, Nature.

[14]  P. Frade,et al.  The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance , 2016, The ISME Journal.

[15]  S. Gilbert,et al.  Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes , 2016, mSystems.

[16]  Robin Patel,et al.  Improved Diagnosis of Prosthetic Joint Infection by Culturing Periprosthetic Tissue Specimens in Blood Culture Bottles , 2016, mBio.

[17]  K. Barott,et al.  Stable and sporadic symbiotic communities of coral and algal holobionts , 2015, The ISME Journal.

[18]  Bas E. Dutilh,et al.  SUPER-FOCUS: a tool for agile functional analysis of shotgun metagenomic data , 2015, Bioinform..

[19]  M. Sweet,et al.  Age-Related Shifts in Bacterial Diversity in a Reef Coral , 2015, PloS one.

[20]  F. Thompson,et al.  Microbial and sponge loops modify fish production in phase-shifting coral reefs. , 2015, Environmental microbiology.

[21]  C. Suttle,et al.  Metagenomic characterization of viral communities in corals: mining biological signal from methodological noise. , 2015, Environmental microbiology.

[22]  E. Hemond,et al.  Diurnal and nocturnal transcriptomic variation in the Caribbean staghorn coral, Acropora cervicornis , 2015, Molecular ecology.

[23]  M. Martinez-Bakker,et al.  The influence of biological rhythms on host-parasite interactions. , 2015, Trends in ecology & evolution.

[24]  Ashley Shade,et al.  Temporal patterns of rarity provide a more complete view of microbial diversity. , 2015, Trends in microbiology.

[25]  Ruth D Gates,et al.  The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts , 2015, The ISME Journal.

[26]  P. Bongaerts,et al.  Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix , 2015, The ISME Journal.

[27]  M. Medina,et al.  Microbes in the coral holobiont: partners through evolution, development, and ecological interactions , 2015, Front. Cell. Infect. Microbiol..

[28]  Forest Rohwer,et al.  Unraveling the Unseen Players in the Ocean - A Field Guide to Water Chemistry and Marine Microbiology , 2014, Journal of visualized experiments : JoVE.

[29]  F. Thompson,et al.  Microbiota of the Major South Atlantic Reef Building Coral Mussismilia , 2014, Microbial Ecology.

[30]  J. Bythell,et al.  Experimental antibiotic treatment identifies potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis , 2014, Proceedings of the Royal Society B: Biological Sciences.

[31]  Bas E. Dutilh,et al.  FOCUS: an alignment-free model to identify organisms in metagenomes using non-negative least squares , 2014, PeerJ.

[32]  R. Stocker,et al.  A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals , 2013, The ISME Journal.

[33]  Oren Levy,et al.  Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. , 2014, Marine genomics.

[34]  R. Kikuchi,et al.  Tolerance of Brazilian brain coral Mussismilia braziliensis to sediment and organic matter inputs. , 2013, Marine pollution bulletin.

[35]  F. Rohwer,et al.  Visualization of oxygen distribution patterns caused by coral and algae , 2013, PeerJ.

[36]  Craig E. Nelson,et al.  Coupled changes in oxygen concentration and pH caused by metabolism of benthic coral reef organisms , 2013 .

[37]  T. Torres,et al.  Bacterial communities and species-specific associations with the mucus of Brazilian coral species , 2013, Scientific Reports.

[38]  N. Webster,et al.  Ocean acidification reduces induction of coral settlement by crustose coralline algae , 2012, Global change biology.

[39]  Fabiano L. Thompson,et al.  Metagenomic Analysis of Healthy and White Plague-Affected Mussismilia braziliensis Corals , 2013, Microbial Ecology.

[40]  K. Barott,et al.  Unseen players shape benthic competition on coral reefs. , 2012, Trends in microbiology.

[41]  Rodolfo Paranhos,et al.  Abrolhos Bank Reef Health Evaluated by Means of Water Quality, Microbial Diversity, Benthic Cover, and Fish Biomass Data , 2012, PloS one.

[42]  F. Azam,et al.  Corals shed bacteria as a potential mechanism of resilience to organic matter enrichment , 2011, The ISME Journal.

[43]  Katherine H. Huang,et al.  Structure, Function and Diversity of the Healthy Human Microbiome , 2012, Nature.

[44]  V. Paul,et al.  Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides , 2011, The ISME Journal.

[45]  C. Castro,et al.  Four-year monthly sediment deposition on turbid southwestern Atlantic coral reefs, with a comparison of benthic assemblages , 2012 .

[46]  N. Moran,et al.  Extreme genome reduction in symbiotic bacteria , 2011, Nature Reviews Microbiology.

[47]  Craig E. Nelson,et al.  Effects of Coral Reef Benthic Primary Producers on Dissolved Organic Carbon and Microbial Activity , 2011, PloS one.

[48]  C. Wild,et al.  Biology and ecology of coral mucus release , 2011 .

[49]  Manuel Porcar,et al.  Complete Genome Sequence of “Candidatus Tremblaya princeps” Strain PCVAL, an Intriguing Translational Machine below the Living-Cell Status , 2011, Journal of bacteriology.

[50]  J. Bythell,et al.  Development of Bacterial Biofilms on Artificial Corals in Comparison to Surface-Associated Microbes of Hard Corals , 2011, PloS one.

[51]  R. Edwards,et al.  Fast Identification and Removal of Sequence Contamination from Genomic and Metagenomic Datasets , 2011, PloS one.

[52]  Robert A. Edwards,et al.  Quality control and preprocessing of metagenomic datasets , 2011, Bioinform..

[53]  O. Hoegh-Guldberg,et al.  Complex Diel Cycles of Gene Expression in Coral-Algal Symbiosis , 2011, Science.

[54]  H. Elifantz,et al.  The impact of reduced pH on the microbial community of the coral Acropora eurystoma , 2011, The ISME Journal.

[55]  J. Bythell,et al.  Bacterial assemblages differ between compartments within the coral holobiont , 2011, Coral Reefs.

[56]  J. Bythell,et al.  Temporal and spatial patterns in waterborne bacterial communities of an island reef system , 2010 .

[57]  Forest Rohwer,et al.  TagCleaner: Identification and removal of tag sequences from genomic and metagenomic datasets , 2010, BMC Bioinformatics.

[58]  L. Martinelli,et al.  Lignin phenols used to infer organic matter sources to Sepetiba Bay – RJ, Brasil , 2010 .

[59]  F. Thompson,et al.  Bacterial Community Associated with Healthy and Diseased Reef Coral Mussismilia hispida from Eastern Brazil , 2010, Microbial Ecology.

[60]  E. Dinsdale,et al.  Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? , 2010, Trends in microbiology.

[61]  C. Brussaard Quantification of aquatic viruses by flow cytometry , 2016 .

[62]  C. D. Harvell,et al.  Microbial Disease and the Coral Holobiont , 2022 .

[63]  J. Erez,et al.  In situ diel cycles of photosynthesis and calcification in hermatypic corals , 2009 .

[64]  Danielle M. Winget,et al.  Diel and daily fluctuations in virioplankton production in coastal ecosystems. , 2009, Environmental microbiology.

[65]  F. Azam,et al.  Resilience of Coral-Associated Bacterial Communities Exposed to Fish Farm Effluent , 2009, PloS one.

[66]  F. Thompson,et al.  Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia braziliensis , 2009, Journal of applied microbiology.

[67]  M. Martindale,et al.  The onset of microbial associations in the coral Pocillopora meandrina , 2009, The ISME Journal.

[68]  Andreas Wilke,et al.  phylogenetic and functional analysis of metagenomes , 2022 .

[69]  E. Rosenberg,et al.  Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. , 2008, FEMS microbiology reviews.

[70]  Rick L. Stevens,et al.  Functional metagenomic profiling of nine biomes , 2008, Nature.

[71]  Florent E. Angly,et al.  Microbial Ecology of Four Coral Atolls in the Northern Line Islands , 2008, PloS one.

[72]  K. Ritchie Regulation of microbial populations by coral surface mucus and mucus-associated bacteria , 2006 .

[73]  S. Nee,et al.  Quantifying the roles of immigration and chance in shaping prokaryote community structure. , 2006, Environmental microbiology.

[74]  Z. Dubinsky,et al.  Diel `tuning' of coral metabolism: physiological responses to light cues , 2006, Journal of Experimental Biology.

[75]  J. Bythell,et al.  Perspectives on mucus secretion in reef corals , 2005 .

[76]  C. Wild,et al.  Influence of coral mucus on nutrient fluxes in carbonate sands , 2005 .

[77]  Z. M. Leão,et al.  A relic coral fauna threatened by global changes and human activities, Eastern Brazil. , 2005, Marine pollution bulletin.

[78]  M. Hidaka,et al.  Diel fluctuations of mycosporine-like amino acids in shallow-water scleractinian corals , 2004 .

[79]  M. Weinbauer,et al.  Diel cycles in viral infection of bacterioplankton in the North Sea , 2004 .

[80]  Markus Huettel,et al.  Coral mucus functions as an energy carrier and particle trap in the reef ecosystem , 2004, Nature.

[81]  C. Brussaard Optimization of Procedures for Counting Viruses by Flow Cytometry , 2004, Applied and Environmental Microbiology.

[82]  Frederick M. Chester,et al.  Hybrid fracture and the transition from extension fracture to shear fracture , 2004, Nature.

[83]  C. Crossland In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes , 1987, Coral Reefs.

[84]  P. Dixon VEGAN, a package of R functions for community ecology , 2003 .

[85]  F. V. AraÚjo,et al.  Flow cytometry assessment of bacterioplankton in tropical marine environments. , 2003, Journal of microbiological methods.

[86]  N. Knowlton,et al.  Diversity and distribution of coral-associated bacteria , 2002 .

[87]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[88]  Brian H. McArdle,et al.  FITTING MULTIVARIATE MODELS TO COMMUNITY DATA: A COMMENT ON DISTANCE‐BASED REDUNDANCY ANALYSIS , 2001 .

[89]  K. Fabricius,et al.  Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. , 2000, Journal of experimental marine biology and ecology.

[90]  T. Thingstad Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems , 2000 .

[91]  Manfred Ehrhardt,et al.  Methods of seawater analysis , 1999 .

[92]  D. Grasso,et al.  Flow cytometry. , 1998, Methods in molecular medicine.

[93]  N. Shashar,et al.  Hydromechanical boundary layers over a coral reef , 1996 .

[94]  L. Richardson,et al.  Oxygen and sulfide dynamics in a horizontally migrating cyanobacterial mat: Black band disease of corals , 1995 .

[95]  H. Kayanne,et al.  Diurnal Changes in the Partial Pressure of Carbon Dioxide in Coral Reef Water , 1995, Science.

[96]  Sunny C. Jiang,et al.  Seasonal and Diel Abundance of Viruses and Occurrence of Lysogeny/Bacteriocinogeny in the Marine Environment , 1994 .

[97]  N. Shashar,et al.  Extreme Diel Fluctuations of Oxygen in Diffusive Boundary Layers Surrounding Stony Corals. , 1993, The Biological bulletin.

[98]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[99]  D. Taylor,et al.  Light-enhanced calcification, and the role of oxidative phosphorylation in calcification of the coral Acropora Cervicornis , 1975, Proceedings of the Royal Society of London. Series B. Biological Sciences.