Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · mBio (Online)
 [1];  [2];  [3];  [4];  [3];  [5];  [6];  [7];  [6];  [6]
  1. San Diego State Univ., CA (United States); Univ. of California, Davis, CA (United States)
  2. San Diego State Univ., CA (United States); Brown Univ., Providence, RI (United States)
  3. San Diego State Univ., CA (United States)
  4. Indiana Univ., Bloomington, IN (United States). National Center for Genome Analysis Support, Pervasive Inst. of Technology
  5. San Diego State Univ., CA (United States); Stanford Univ., CA (United States)
  6. San Diego State Univ., CA (United States); San Diego State Univ., CA (United States). Viral Information Inst.
  7. Bermuda Inst. of Ocean Sciences, St. George's (Bermuda)
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. 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.
Research Organization:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDOE National Nuclear Security Administration (NNSA)
Grant/Contract Number:
AC52-07NA27344
OSTI ID:
1775027
Report Number(s):
LLNL-JRNL--814122; 1022596
Journal Information:
mBio (Online), Journal Name: mBio (Online) Journal Issue: 2 Vol. 11; ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)Copyright Statement
Country of Publication:
United States
Language:
English

References (116)

Microbial indicators as a diagnostic tool for assessing water quality and climate stress in coral reef ecosystems journal March 2017
Variability in Microbial Community Composition and Function Between Different Niches Within a Coral Reef journal January 2014
Antagonistic Interactions and Biofilm Forming Capabilities Among Bacterial Strains Isolated from the Egg Surfaces of Lake Sturgeon (Acipenser fulvescens) journal July 2017
CPR and DPANN Have an Overlooked Role in Corals’ Microbial Community Structure journal March 2021
Next generation sequencing reveals limitation of qPCR methods in quantifying emerging antibiotic resistance genes (ARGs) in the environment journal March 2021
Reproductive ecology and early life history traits of the brooding coral, Porites astreoides, from shallow to mesophotic zones journal February 2018
Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals journal August 2001
Ecological network analysis: network construction journal October 2007
The effect of dissolved nickel and copper on the adult coral Acropora muricata and its microbiome journal July 2019
Making a microbiome: the many determinants of host-associated microbial community composition journal February 2017
Some unique properties of eigenvector centrality journal October 2007
Disentangling Interactions in the Microbiome: A Network Perspective journal March 2017
The impact of reduced pH on the microbial community of the coral Acropora eurystoma journal July 2010
Marine bacterial, archaeal and protistan association networks reveal ecological linkages journal March 2011
Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists journal November 2013
Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix journal February 2015
Functional metagenomic profiling of nine biomes journal March 2008
The evolution of the host microbiome as an ecosystem on a leash journal August 2017
Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence journal May 2015
Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales journal June 2016
Bacterial community dynamics are linked to patterns of coral heat tolerance journal February 2017
Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes journal March 2009
Global microbialization of coral reefs journal April 2016
Dynamic models of the complex microbial metapopulation of lake mendota journal March 2016
Unravelling the effects of the environment and host genotype on the gut microbiome journal March 2011
Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny journal November 2018
Mathematical modeling of primary succession of murine intestinal microbiota journal December 2013
Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors journal June 2014
Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching journal July 1999
Factoring and weighting approaches to status scores and clique identification journal January 1972
Quality control and preprocessing of metagenomic datasets journal January 2011
Successive shifts in the microbial community of the surface mucus layer and tissues of the coral Acropora muricata under thermal stress journal November 2015
From hairballs to hypotheses–biological insights from microbial networks journal July 2018
Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases journal March 2013
De novo bacterial genome sequencing: Millions of very short reads assembled on a desktop computer journal February 2008
Disentangling causation: complex roles of coral-associated microorganisms in disease: Disentangling coral disease causation journal November 2017
Caribbean corals house shared and host-specific microbial symbionts over time and space: Specificity and overlap in coral microbiomes journal June 2016
Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching journal November 2013
Distinct biogeographical patterns of marine bacterial taxonomy and functional genes: Biogeography of bacterial taxonomy and functional genes journal October 2016
Catastrophic mortality on inshore coral reefs of the Florida Keys due to severe low-temperature stress journal July 2011
A predictive model for combined temperature and water activity on microbial growth during the growth phase journal November 1989
The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach journal March 1996
Metagenomic analysis of the microbial community associated with the coral Porites astreoides journal November 2007
Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle journal November 2008
Antagonistic interactions among coral-associated bacteria journal January 2010
Environmental controls on modern scleractinian coral and reef-scale calcification journal November 2017
Convenient Model To Describe the Combined Effects of Temperature and pH on Microbial Growth. journal January 1995
Relationship between temperature and growth rate of bacterial cultures. journal January 1982
Avian Influenza Dynamics Under Periodic Environmental Conditions journal January 2015
Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems journal September 2016
Molecular ecological network analyses journal January 2012
Microbes, metagenomes and marine mammals: enabling the next generation of scientist to enter the genomic era journal January 2013
Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata journal September 2017
Microbial indicators of environmental perturbations in coral reef ecosystems journal June 2019
Microbial Ecology of Four Coral Atolls in the Northern Line Islands journal February 2008
Elevated temperature drives kelp microbiome dysbiosis, while elevated carbon dioxide induces water microbiome disruption journal February 2018
A Set of Measures of Centrality Based on Betweenness journal March 1977
Changes in Caribbean coral disease prevalence after the 2005 bleaching event journal November 2009
Perspectives on mucus secretion in reef corals journal January 2005
Multivariate analysis of functional metagenomes journal January 2013
Molecular characterization of vulnibactin biosynthesis in Vibrio vulnificus indicates the existence of an alternative siderophore journal January 2014
Deciphering microbial interactions and detecting keystone species with co-occurrence networks journal May 2014
Commentary: Microbial Small Talk: Volatiles in Fungal–Bacterial Interactions journal January 2017
Planula release and reproductive seasonality of the scleractinian coral Porites astreoides in Bermuda, a high-latitude reef journal January 2011
Coral Disease, Environmental Drivers, and the Balance Between Coral and Microbial Associates journal March 2007
Influence of coral and algal exudates on microbially mediated reef metabolism journal January 2013
Aura-biomes are present in the water layer above coral reef benthic macro-organisms journal January 2017
FOCUS: an alignment-free model to identify organisms in metagenomes using non-negative least squares journal January 2014
An Unexpected Correlation between Cardinal Temperatures of Microbial Growth Highlighted by a New Model journal June 1993
Biology and Ecology of Corals and Fishes on the Bermuda Platform book January 2013
Relationships between temperature, bleaching and white syndrome on the Great Barrier Reef journal August 2012
Variation in larval properties of the Atlantic brooding coral Porites astreoides between different reef sites in Bermuda journal January 2017
Temperature affects microbial abundance, activity and interactions in anaerobic digestion journal June 2016
Incidence of lesions on Fungiidae corals in the eastern Red Sea is related to water temperature and coastal pollution journal July 2014
Centrality and network flow journal January 2005
Nitrogen cycling in corals: the key to understanding holobiont functioning? journal August 2015
Small change, big difference: Sea surface temperature distributions for tropical coral reef ecosystems, 1950-2011: CHANGING TROPICAL SST DISTRIBUTIONS journal September 2012
Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae journal October 2010
The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance journal March 2016
DMSP biosynthesis by an animal and its role in coral thermal stress response journal October 2013
Bright spots among the world’s coral reefs journal June 2016
Critical Assessment of Metagenome Interpretation—a benchmark of metagenomics software journal October 2017
Stress and stability: applying the Anna Karenina principle to animal microbiomes journal August 2017
Cold induces acute stress but heat is ultimately more deleterious for the reef-building coral Acropora yongei journal February 2012
Topological distortion and reorganized modular structure of gut microbial co-occurrence networks in inflammatory bowel disease journal May 2016
Factoring and weighting approaches to status scores and clique identification journal January 1972
PEAR: a fast and accurate Illumina Paired-End reAd mergeR journal October 2013
Microbial processes driving coral reef organic carbon flow journal May 2017
Bacterioplankton community resilience to ocean acidification: evidence from microbial network analysis journal November 2015
Chlamydial seasonal dynamics and isolation of ‘ C andidatus  Neptunochlamydia vexilliferae’ from a Tyrrhenian coastal lake: Environmental chlamydiae in Lago di Paola ( Latium , Italy) journal December 2015
Persistent shifts in Caribbean coral microbiota are linked to the 2010 warm thermal anomaly: Coral bacteria shift with species and temperature journal April 2015
The skin microbiome of the common thresher shark ( Alopias vulpinus ) has low taxonomic and gene function β-diversity: Skin microbiome of the common thresher shark journal June 2017
Coral microbiome database: Integration of sequences reveals high diversity and relatedness of coral‐associated microbes journal September 2018
Metagenomic analysis of stressed coral holobionts journal August 2009
Coral mucus-associated bacteria: a possible first line of defense: Coral mucus-associated bacteria journal March 2009
The amphibian skin-associated microbiome across species, space and life history stages journal October 2013
Spatial and temporal patterns of mass bleaching of corals in the Anthropocene journal January 2018
Convenient Model To Describe the Combined Effects of Temperature and pH on Microbial Growth. journal January 1995
Relationship between temperature and growth rate of bacterial cultures. journal January 1982
Distinguishing between Microbial Habitats Unravels Ecological Complexity in Coral Microbiomes journal October 2016
Rhodoliths holobionts in a changing ocean: host-microbes interactions mediate coralline algae resilience under ocean acidification journal September 2018
Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes journal August 2015
Resilience of Coral-Associated Bacterial Communities Exposed to Fish Farm Effluent journal October 2009
Microbiome dynamics of two differentially resilient corals journal November 2018
Diversity and distribution of coral-associated bacteria journal January 2002
Regulation of microbial populations by coral surface mucus and mucus-associated bacteria journal September 2006
High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems journal July 2018
Environmental disruption of host–microbe co-adaptation as a potential driving force in evolution journal June 2014
On the Importance of the Microbiome and Pathobiome in Coral Health and Disease journal January 2017
Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean journal July 2017
Responses of Coral-Associated Bacterial Communities to Local and Global Stressors journal August 2017
The engine of the reef: photobiology of the coral–algal symbiosis journal August 2014
Beneficial Microorganisms for Corals (BMC): Proposed Mechanisms for Coral Health and Resilience journal March 2017
Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata collection January 2017
Microbial indicators of environmental perturbations in coral reef ecosystems collection January 2019
Alien vs. predator: bacterial challenge alters coral microbiomes unless controlled by Halobacteriovorax predators journal January 2017

Cited By (1)


Similar Records

Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale
Journal Article · Sun Aug 14 20:00:00 EDT 2022 · Microbial Ecology · OSTI ID:1883025

Pre-Bleaching Coral Microbiome Is Enriched in Beneficial Taxa and Functions
Journal Article · Wed May 15 20:00:00 EDT 2024 · Microorganisms · OSTI ID:2471180

Spatial Homogeneity of Bacterial Communities Associated with the Surface Mucus Layer of the Reef-Building Coral Acropora palmata
Journal Article · Sun Dec 13 19:00:00 EST 2015 · PLoS ONE · OSTI ID:1904065