Dataset Information

Comparative genome-centric analysis reveals seasonal variation in the function of coral reef microbiomes.

ABSTRACT: Microbially mediated processes contribute to coral reef resilience yet, despite extensive characterisation of microbial community variation following environmental perturbation, the effect on microbiome function is poorly understood. We undertook metagenomic sequencing of sponge, macroalgae and seawater microbiomes from a macroalgae-dominated inshore coral reef to define their functional potential and evaluate seasonal shifts in microbially mediated processes. In total, 125 high-quality metagenome-assembled genomes were reconstructed, spanning 15 bacterial and 3 archaeal phyla. Multivariate analysis of the genomes relative abundance revealed changes in the functional potential of reef microbiomes in relation to seasonal environmental fluctuations (e.g. macroalgae biomass, temperature). For example, a shift from Alphaproteobacteria to Bacteroidota-dominated seawater microbiomes occurred during summer, resulting in an increased genomic potential to degrade macroalgal-derived polysaccharides. An 85% reduction of Chloroflexota was observed in the sponge microbiome during summer, with potential consequences for nutrition, waste product removal, and detoxification in the sponge holobiont. A shift in the Firmicutes:Bacteroidota ratio was detected on macroalgae over summer with potential implications for polysaccharide degradation in macroalgal microbiomes. These results highlight that seasonal shifts in the dominant microbial taxa alter the functional repertoire of host-associated and seawater microbiomes, and highlight how environmental perturbation can affect microbially mediated processes in coral reef ecosystems.

SUBMITTER: Glasl B

PROVIDER: S-EPMC7242418 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Comparative genome-centric analysis reveals seasonal variation in the function of coral reef microbiomes.

Glasl Bettina B Robbins Steven S Frade Pedro R PR Marangon Emma E Laffy Patrick W PW Bourne David G DG Webster Nicole S NS

The ISME journal 20200302 6

Microbially mediated processes contribute to coral reef resilience yet, despite extensive characterisation of microbial community variation following environmental perturbation, the effect on microbiome function is poorly understood. We undertook metagenomic sequencing of sponge, macroalgae and seawater microbiomes from a macroalgae-dominated inshore coral reef to define their functional potential and evaluate seasonal shifts in microbially mediated processes. In total, 125 high-quality metageno ...[more]

PMID: 32123297

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Project description:Reef organisms influence microorganisms within the surrounding seawater, yet the spatial and temporal dynamics of seawater microbial communities located in proximity to corals are rarely investigated. To better understand reef seawater microbial community dynamics over time and space, we collected small-volume seawater samples during the day and night over a 72 hour period from three locations that differed in spatial distance from 5 Porites astreoides coral colonies on a shallow reef in St. John, U.S. Virgin Islands: near-coral (sampled 5 cm horizontally from each colony), reef-depth (sampled 2 m above each colony) and surface seawater (sampled 1 m from the seawater surface). At all time points and locations, we quantified abundances of microbial cells, sequenced small subunit rRNA genes of bacterial and archaeal communities, and measured inorganic nutrient concentrations. Prochlorococcus and Synechococcus cells were consistently elevated at night compared to day and these abundances changed over time, corresponding with temperature, nitrite, and silicate concentrations. During the day, bacterial and archaeal alpha diversity was significantly higher in reef-depth and near-coral seawater compared to the surface seawater, signifying that the reef influences the diversity of the seawater microorganisms. At night, alpha diversity decreased across all samples, suggesting that photosynthesis may favor a more taxonomically diverse community. While Prochlorococcus exhibited consistent temporal rhythmicity, additional taxa were enriched in reef seawater at night compared to day or in reef-depth compared to surface seawater based on their normalized sequence counts. There were some significant differences in nutrient concentrations and cell abundances between reef-depth and near-coral seawater but no clear trends. This study demonstrates that temporal variation supersedes small-scale spatial variation in proximity to corals in reef seawater microbial communities. As coral reefs continue to change in benthic composition worldwide, monitoring microbial composition in response to temporal changes and environmental fluctuations will help discern normal variability from longer lasting changes attributed to anthropogenic stressors and global climate change.

Project description:The metabolic rate of consumers is a key driver of ecosystem dynamics. On coral reefs, herbivorous echinoids consume fleshy algae, facilitating the growth of reef-building calcified organisms; however, little is known about differences among species in their metabolic and functional ecology. Here, we used log-linear (log-log) regression models to examine the allometric scaling of mass and routine metabolic rate for five common herbivorous echinoids on a Hawaiian coral reef: Echinothrix calamaris, E. diadema, Echinometra matthaei, Heterocentrotus mammillatus, and Tripneustes gratilla. Scaling relationships were then contrasted with empirical observations of echinoid ecology and general metabolic theory to broaden our understanding of diversity in the metabolic and functional ecology of tropical herbivorous echinoids.Test diameter and species explained 98% of the variation in mass, and mass and species explained 92.4% and 87.5% of the variation in individual (I) and mass-specific (B) metabolic rates, respectively. Scaling exponents did not differ for mass or metabolism; however, normalizing constants differed significantly among species. Mass varied as the cube of test diameter (b = 2.9), with HM exhibiting a significantly higher normalizing constant than other species, likely due to its heavily-calcified spines and skeleton. Individual metabolic rate varied approximately as the 2/5 power of mass (? = 0.44); significantly smaller than the 3/4 universal scaling coefficient, but inclusive of 2/3 scaling. E. calamaris and H. mammillatus exhibited the lowest normalizing constants, corresponding with their slow-moving, cryptic, rock-boring life-history. In contrast, E. calamaris, E. diadema, and T. gratilla, exhibited higher metabolic rates, likely reflecting their higher levels of activity and ability to freely browse for preferred algae due to chemical anti-predator defenses. Thus, differences in metabolic scaling appeared to correspond with differences in phylogeny, behavior, and ecological function. Such comparative metabolic assessments are central to informing theory, ecological models, and the effective management of ecosystems.

Dataset Information

Comparative genome-centric analysis reveals seasonal variation in the function of coral reef microbiomes.

Publications

Comparative genome-centric analysis reveals seasonal variation in the function of coral reef microbiomes.

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