Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network

Coral microbiome dysbiosis (i.e., shifts in the microbial community structure or complete loss of microbial symbionts) caused by environmental changes is a key player in the decline of coral health worldwide. Multiple factors in the water column and the surrounding biological community influence the dynamics of the coral microbiome. However, by including only temperature as an external factor, our model proved to be successful in describing the microbial community associated with the surface mucus layer (SML) of the coral P. strigosa. The dynamic model developed and validated in this study is a potential tool to predict the coral microbiome under different temperature conditions. ABSTRACT Host-associated microbial communities are shaped by extrinsic and intrinsic factors to the holobiont organism. Environmental factors and microbe-microbe interactions act simultaneously on the microbial community structure, making the microbiome dynamics challenging to predict. The coral microbiome is essential to the health of coral reefs and sensitive to environmental changes. Here, we develop a dynamic model to determine the microbial community structure associated with the surface mucus layer (SML) of corals using temperature as an extrinsic factor and microbial network as an intrinsic factor. The model was validated by comparing the predicted relative abundances of microbial taxa to the relative abundances of microbial taxa from the sample data. The SML microbiome from Pseudodiploria strigosa was collected across reef zones in Bermuda, where inner and outer reefs are exposed to distinct thermal profiles. A shotgun metagenomics approach was used to describe the taxonomic composition and the microbial network of the coral SML microbiome. By simulating the annual temperature fluctuations at each reef zone, the model output is statistically identical to the observed data. The model was further applied to six scenarios that combined different profiles of temperature and microbial network to investigate the influence of each of these two factors on the model accuracy. The SML microbiome was best predicted by model scenarios with the temperature profile that was closest to the local thermal environment, regardless of the microbial network profile. Our model shows that the SML microbiome of P. strigosa in Bermuda is primarily structured by seasonal fluctuations in temperature at a reef scale, while the microbial network is a secondary driver. IMPORTANCE Coral microbiome dysbiosis (i.e., shifts in the microbial community structure or complete loss of microbial symbionts) caused by environmental changes is a key player in the decline of coral health worldwide. Multiple factors in the water column and the surrounding biological community influence the dynamics of the coral microbiome. However, by including only temperature as an external factor, our model proved to be successful in describing the microbial community associated with the surface mucus layer (SML) of the coral P. strigosa. The dynamic model developed and validated in this study is a potential tool to predict the coral microbiome under different temperature conditions.

[1]  P. Greenfield,et al.  The effect of dissolved nickel and copper on the adult coral Acropora muricata and its microbiome. , 2019, Environmental pollution.

[2]  T. Thomas,et al.  Microbial indicators of environmental perturbations in coral reef ecosystems , 2019, Microbiome.

[3]  M. Huggett,et al.  Coral microbiome database: Integration of sequences reveals high diversity and relatedness of coral‐associated microbes , 2018, Environmental microbiology reports.

[4]  L. Richardson,et al.  Microbiome dynamics of two differentially resilient corals. , 2018, Diseases of aquatic organisms.

[5]  Jesse R. Zaneveld,et al.  Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny , 2018, Nature Communications.

[6]  E. Dinsdale,et al.  Rhodoliths holobionts in a changing ocean: host-microbes interactions mediate coralline algae resilience under ocean acidification , 2018, BMC Genomics.

[7]  Karoline Faust,et al.  From hairballs to hypotheses–biological insights from microbial networks , 2018, FEMS microbiology reviews.

[8]  M. Vayssier-Taussat,et al.  High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems , 2018, Front. Cell. Infect. Microbiol..

[9]  R. Jiang,et al.  Prediction of enhancer-promoter interactions via natural language processing , 2018, BMC Genomics.

[10]  G. Goodbody-Gringley,et al.  Reproductive ecology and early life history traits of the brooding coral, Porites astreoides, from shallow to mesophotic zones , 2018, Coral Reefs.

[11]  Michael Doane,et al.  Elevated temperature drives kelp microbiome dysbiosis, while elevated carbon dioxide induces water microbiome disruption , 2018, PloS one.

[12]  D. Bourne,et al.  Disentangling causation: complex roles of coral‐associated microorganisms in disease , 2018, Environmental microbiology.

[13]  Ryan J. Lowe,et al.  Spatial and temporal patterns of mass bleaching of corals in the Anthropocene , 2018, Science.

[14]  Mario Lebrato,et al.  Environmental controls on modern scleractinian coral and reef-scale calcification , 2017, Science Advances.

[15]  F. Stewart,et al.  Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata , 2017, Microbiome.

[16]  Jesse R. Zaneveld,et al.  Stress and stability: applying the Anna Karenina principle to animal microbiomes , 2017, Nature Microbiology.

[17]  E. Dinsdale,et al.  Aura-biomes are present in the water layer above coral reef benthic macro-organisms , 2017, PeerJ.

[18]  M. Garren,et al.  Responses of Coral-Associated Bacterial Communities to Local and Global Stressors , 2017, Front. Mar. Sci..

[19]  K. Foster,et al.  The evolution of the host microbiome as an ecosystem on a leash , 2017, Nature.

[20]  Amy Apprill,et al.  Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean , 2017, Front. Mar. Sci..

[21]  E. Dinsdale,et al.  Microbial processes driving coral reef organic carbon flow , 2017, FEMS microbiology reviews.

[22]  Stephen R. Lindemann,et al.  Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach , 2017, Front. Microbiol..

[23]  Philip D. Blood,et al.  Critical Assessment of Metagenome Interpretation—a benchmark of metagenomics software , 2017, Nature Methods.

[24]  Jesse R. Zaneveld,et al.  Alien vs. predator: bacterial challenge alters coral microbiomes unless controlled by Halobacteriovorax predators , 2017, PeerJ.

[25]  E. Dinsdale,et al.  The skin microbiome of the common thresher shark (Alopias vulpinus) has low taxonomic and gene function &bgr;‐diversity , 2017, Environmental microbiology reports.

[26]  P. Quazuguel,et al.  Genomic organization and spatio-temporal expression of the hemoglobin genes in European sea bass (Dicentrarchus labrax) , 2017 .

[27]  D. Bourne,et al.  Microbial indicators as a diagnostic tool for assessing water quality and climate stress in coral reef ecosystems , 2017 .

[28]  R. Peixoto,et al.  Beneficial Microorganisms for Corals (BMC): Proposed Mechanisms for Coral Health and Resilience , 2017, Front. Microbiol..

[29]  S. Palumbi,et al.  Bacterial community dynamics are linked to patterns of coral heat tolerance , 2017, Nature Communications.

[30]  F. Kong,et al.  Moraxella catarrhalis Macrolide-Resistant Isolates Are Highly Concentrated in Two MLST Clonal Complexes -CCN10 and CC363 , 2017, Front. Microbiol..

[31]  E. Dinsdale,et al.  Distinct biogeographical patterns of marine bacterial taxonomy and functional genes , 2017 .

[32]  Karen L. Adair,et al.  Making a microbiome: the many determinants of host-associated microbial community composition. , 2017, Current opinion in microbiology.

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

[34]  Jochen Horstmann,et al.  HF Radar Activity in European Coastal Seas: Next Steps toward a Pan-European HF Radar Network , 2017, Front. Mar. Sci..

[35]  Mehdi Layeghifard,et al.  Disentangling Interactions in the Microbiome: A Network Perspective , 2016, Trends in Microbiology.

[36]  T. Marsh,et al.  Antagonistic Interactions and Biofilm Forming Capabilities Among Bacterial Strains Isolated from the Egg Surfaces of Lake Sturgeon (Acipenser fulvescens) , 2017, Microbial Ecology.

[37]  Matthew T. Costa,et al.  Variation in larval properties of the Atlantic brooding coral Porites astreoides between different reef sites in Bermuda , 2017, Coral Reefs.

[38]  A. Santoro,et al.  Distinguishing between Microbial Habitats Unravels Ecological Complexity in Coral Microbiomes , 2016, mSystems.

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

[40]  R. Amann,et al.  Chlamydial seasonal dynamics and isolation of 'Candidatus Neptunochlamydia vexilliferae' from a Tyrrhenian coastal lake. , 2016, Environmental microbiology.

[41]  Nathaniel D. Chu,et al.  Caribbean corals house shared and host-specific microbial symbionts over time and space. , 2016, Environmental microbiology reports.

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

[43]  Jiabao Li,et al.  Temperature affects microbial abundance, activity and interactions in anaerobic digestion. , 2016, Bioresource technology.

[44]  Danielle S. Bassett,et al.  Topological distortion and reorganized modular structure of gut microbial co-occurrence networks in inflammatory bowel disease , 2016, Scientific Reports.

[45]  Craig E. Nelson,et al.  Global microbialization of coral reefs , 2016, Nature Microbiology.

[46]  Eberhard O Voit,et al.  Dynamic models of the complex microbial metapopulation of lake mendota , 2016, npj Systems Biology and Applications.

[47]  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.

[48]  B. Baker,et al.  Correction: Corrigendum: Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea , 2016 .

[49]  Jizhong Zhou,et al.  Bacterioplankton community resilience to ocean acidification: evidence from microbial network analysis , 2016 .

[50]  David Mouillot,et al.  Bright spots among the world’s coral reefs , 2016, Nature.

[51]  Sen-Lin Tang,et al.  Successive shifts in the microbial community of the surface mucus layer and tissues of the coral Acropora muricata under thermal stress. , 2015, FEMS microbiology ecology.

[52]  C. Wild,et al.  Nitrogen cycling in corals: the key to understanding holobiont functioning? , 2015, Trends in microbiology.

[53]  K. Theis,et al.  Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes , 2015, PLoS biology.

[54]  Joleah B. Lamb,et al.  Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence , 2015 .

[55]  O. Koren,et al.  Persistent shifts in Caribbean coral microbiota are linked to the 2010 warm thermal anomaly. , 2015, Environmental microbiology reports.

[56]  Lindi M. Wahl,et al.  Avian Influenza Dynamics Under Periodic Environmental Conditions , 2015, SIAM J. Appl. Math..

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

[58]  Melissa S. Roth.  The engine of the reef: photobiology of the coral–algal symbiosis , 2014, Front. Microbiol..

[59]  Michael Kühl,et al.  Spatial patterns and links between microbial community composition and function in cyanobacterial mats , 2014, Front. Microbiol..

[60]  K. Hughen,et al.  Incidence of lesions on Fungiidae corals in the eastern Red Sea is related to water temperature and coastal pollution. , 2014, Marine environmental research.

[61]  Craig E. Nelson,et al.  Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors , 2014, Proceedings of the National Academy of Sciences.

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

[63]  Stefanie Widder,et al.  Deciphering microbial interactions and detecting keystone species with co-occurrence networks , 2014, Front. Microbiol..

[64]  Y. Soen.  Environmental disruption of host–microbe co-adaptation as a potential driving force in evolution , 2014, Front. Genet..

[65]  A. Arkin,et al.  Genetic basis for nitrate resistance in Desulfovibrio strains , 2014, Front. Microbiol..

[66]  D. Caron,et al.  Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists , 2013, The ISME Journal.

[67]  R. Knight,et al.  The amphibian skin‐associated microbiome across species, space and life history stages , 2014, Molecular ecology.

[68]  Jesse R Zaneveld,et al.  Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching , 2014, Global change biology.

[69]  Jiajie Zhang,et al.  PEAR: a fast and accurate Illumina Paired-End reAd mergeR , 2013, Bioinform..

[70]  R. Stocker,et al.  Variability in Microbial Community Composition and Function Between Different Niches Within a Coral Reef , 2014, Microbial Ecology.

[71]  Simeone Marino,et al.  Mathematical modeling of primary succession of murine intestinal microbiota , 2013, Proceedings of the National Academy of Sciences.

[72]  B. Willis,et al.  DMSP biosynthesis by an animal and its role in coral thermal stress response , 2013, Nature.

[73]  Timothy T Harkins,et al.  Microbes, metagenomes and marine mammals: enabling the next generation of scientist to enter the genomic era , 2013, BMC Genomics.

[74]  Craig E. Nelson,et al.  Influence of coral and algal exudates on microbially mediated reef metabolism , 2013, PeerJ.

[75]  V. Paul,et al.  Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases , 2013, Proceedings of the Royal Society B: Biological Sciences.

[76]  Robert A. Edwards,et al.  Multivariate Analysis of Functional Metagenomes , 2013, Front. Genet..

[77]  C. Sheppard,et al.  Coral Reefs of the United Kingdom Overseas Territories , 2013 .

[78]  N. Bates,et al.  Threats to coral reefs of Bermuda , 2013 .

[79]  I. Nagelkerken,et al.  Biology and Ecology of Corals and Fishes on the Bermuda Platform , 2013 .

[80]  S. Ban,et al.  Relationships between temperature, bleaching and white syndrome on the Great Barrier Reef , 2012, Coral Reefs.

[81]  J. Lough.  Small change, big difference: Sea surface temperature distributions for tropical coral reef ecosystems, 1950–2011 , 2012 .

[82]  R. Goericke,et al.  Cold induces acute stress but heat is ultimately more deleterious for the reef-building coral Acropora yongei , 2012, Scientific Reports.

[83]  Feng Luo,et al.  Molecular ecological network analyses , 2012, BMC Bioinformatics.

[84]  W. Fitt,et al.  Catastrophic mortality on inshore coral reefs of the Florida Keys due to severe low‐temperature stress , 2011 .

[85]  D. Caron,et al.  Marine bacterial, archaeal and protistan association networks reveal ecological linkages , 2011, The ISME Journal.

[86]  N. Webster,et al.  Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae , 2011, The ISME Journal.

[87]  Ruth Ley,et al.  Unravelling the effects of the environment and host genotype on the gut microbiome , 2011, Nature Reviews Microbiology.

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

[89]  S. J. Putron,et al.  Planula release and reproductive seasonality of the scleractinian coral Porites astreoides in Bermuda, a high-latitude reef , 2011 .

[90]  E. Dinsdale,et al.  Fish or Germs? Microbial Dynamics Associated with Changing Trophic Structures on Coral Reefs , 2011 .

[91]  Wes McKinney,et al.  pandas: a Foundational Python Library for Data Analysis and Statistics , 2011 .

[92]  Zvy Dubinsky,et al.  Coral reefs : an ecosystem in transition , 2011 .

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

[94]  F. Azam,et al.  Antagonistic interactions among coral-associated bacteria. , 2010, Environmental microbiology.

[95]  E. Weil,et al.  Changes in Caribbean coral disease prevalence after the 2005 bleaching event. , 2009, Diseases of aquatic organisms.

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

[97]  Florent E. Angly,et al.  Metagenomic analysis of stressed coral holobionts. , 2009, Environmental microbiology.

[98]  M. Shnit-Orland,et al.  Coral mucus-associated bacteria: a possible first line of defense. , 2009, FEMS microbiology ecology.

[99]  Z. Ning,et al.  Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of GC-biased genomes , 2009, Nature Methods.

[100]  William Revelle,et al.  An overview of the psych package , 2009 .

[101]  N. Siboni,et al.  Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. , 2008, Environmental microbiology.

[102]  David Hernández,et al.  De novo bacterial genome sequencing: millions of very short reads assembled on a desktop computer. , 2008, Genome research.

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

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

[105]  Aric Hagberg,et al.  Exploring Network Structure, Dynamics, and Function using NetworkX , 2008, Proceedings of the Python in Science Conference.

[106]  Forest Rohwer,et al.  Metagenomic analysis of the microbial community associated with the coral Porites astreoides. , 2007, Environmental microbiology.

[107]  Bruce Hannon,et al.  Ecological network analysis : network construction , 2007 .

[108]  Phillip Bonacich,et al.  Some unique properties of eigenvector centrality , 2007, Soc. Networks.

[109]  B. Willis,et al.  Coral disease, environmental drivers, and the balance between coral and microbial associates , 2007 .

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

[111]  Gábor Csárdi,et al.  The igraph software package for complex network research , 2006 .

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

[113]  Stephen P. Borgatti,et al.  Centrality and network flow , 2005, Soc. Networks.

[114]  Elizabeth A. Dinsdale,et al.  Coral Disease on the Great Barrier Reef , 2004 .

[115]  Y. Loya,et al.  Coral Health and Disease , 2004, Springer Berlin Heidelberg.

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

[117]  Mark E. Warner,et al.  Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals , 2001, Coral Reefs.

[118]  E. Dinsdale.  Abundance of black-band disease on corals from one location on the Great Barrier Reef: a comparison with abundance in the Caribbean region , 2000 .

[119]  G. Schmidt,et al.  Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[120]  Mark E. Warner,et al.  The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach , 1996 .

[121]  J P Flandrois,et al.  Convenient Model To Describe the Combined Effects of Temperature and pH on Microbial Growth , 1995, Applied and environmental microbiology.

[122]  J P Flandrois,et al.  An unexpected correlation between cardinal temperatures of microbial growth highlighted by a new model. , 1993, Journal of theoretical biology.

[123]  K. Davey,et al.  A predictive model for combined temperature and water activity on microbial growth during the growth phase. , 1989, The Journal of applied bacteriology.

[124]  J Olley,et al.  Relationship between temperature and growth rate of bacterial cultures , 1982, Journal of bacteriology.

[125]  Leonard M. Freeman,et al.  A set of measures of centrality based upon betweenness , 1977 .

[126]  P. Bonacich.  Factoring and weighting approaches to status scores and clique identification , 1972 .