Metagenomics of Coral Reefs Under Phase Shift and High Hydrodynamics

Abstract

Local and global stressors have affected coral reef ecosystems worldwide. Switches from coral to algal dominance states and microbialization are the major processes underlying the global decline of coral reefs. However, most of the knowledge concerning microbialization has not considered physical disturbances (e.g., typhoons, waves, and currents). Southern Japan reef systems have developed under extreme physical disturbances. Here, we present analyses of a three-year investigation on the coral reefs of Ishigaki Island that comprised benthic and fish surveys, water quality analyses, metagenomics and microbial abundance data. At the four studied sites, inorganic nutrient concentrations were high and exceeded eutrophication thresholds. The dissolved organic carbon (DOC) concentration (up to 233.3 μM) and microbial abundance (up to 2.5 × 10⁵ cell/mL) values were relatively high. The highest vibrio counts coincided with the highest turf cover (∼55-85%) and the lowest coral cover (∼4.4-10.2%) and fish biomass (0.06 individuals/m²). Microbiome compositions were similar among all sites and were dominated by heterotrophs. Our data suggest that a synergic effect among several regional stressors are driving coral decline. In a high hydrodynamics reef environment, high algal/turf cover, stimulated by eutrophication and low fish abundance due to overfishing, promote microbialization. Together with crown-of-thorns starfish (COTS) outbreaks and possible of climate changes impacts, theses coral reefs are likely to collapse.

Keywords: coral reefs; early warning signals; hydrodynamics; local stressors; metagenomics; microbialization; resistence.

FIGURE 1

Modeled wave generated near bottom orbital velocity (m/s) in the area of interest. Example for calm (A) and typhoon (B) wave conditions. Note difference in color bar scales.

FIGURE 2

Coral reefs from Ishigaki Island are impacted at different levels. Yellow and green lines represent coral and algal cover in percentages for the reef sites and years, respectively (A). The first two axes of non-metric multidimensional scaling (nMDS) based on benthic cover (B) and fish abundance (C) show each benthic sample replicate using different colors for sites and different shapes for years. The taxonomic compositions of water metagenomes, heterotrophic bacteria, potential coral pathogenic bacteria, and highly abundant bacteria in turf algae are represented by different colors (D). The asterisk in Cyanobacteria represents the bacterial genera Anabaena, Nostoc, and Trichodesmium (cyanobacteria genera commonly found in turf algae). CFB complex, Cytophaga–Flavobacterium–Bacteroides complex.

FIGURE 3

Ishigaki coral reef and fish community composition structure. (A) Relative coral cover. (B) Relative abundance of fish families. (C) Canonical correspondence analysis (CCA) biplot of benthic cover and fish assemblages of Ishigaki coral reefs. Each replicate is represented by dots in different colors (for sites) and different shapes (for years). Species abbreviations are: CTESTR, Ctenochaetus striatus; STEALT, Stegastes altus; CHLSOR, Chlorurus sordidus; POMLEP, Pomacentrus lepidogenys; CHRMAR, Chromis margaritifer; CHRREX, Chrysiptera rex; CHRATR, Chromis atripectoralis; ABUSEX, Abudefduf sexfasciatus; THALUT, Thalassoma lutescens; THAHAR, Thalassoma hardwicke; GOMVAR, Gomphosus varius; LABDIM, Labroides dimidiatus; ZEBSCO, Zebrasoma scopas.

FIGURE 4

The microbial communities of Ishigaki coral reef seawater have similar genetic compositions. Cladograms representing the fraction of cross-contigs (i.e., shared contigs that contain reads from two or more metagenomes) after cross-assembly.