Abstract

As coral reef habitats decline worldwide, some reefs are transitioning from coral- to algal-dominated benthos with the exact cause for this shift remaining elusive. Increases in the abundance of microbes in the water column has been correlated with an increase in coral disease and reduction in coral cover. Here we investigated how multiple reef organisms influence microbial communities in the surrounding water column. Our study consisted of a field assessment of microbial communities above replicate patches dominated by a single macro-organism. Metagenomes were constructed from 20 L of water above distinct macro-organisms, including (1) the coral Mussismilia braziliensis, (2) fleshy macroalgae (Stypopodium, Dictota and Canistrocarpus), (3) turf algae, and (4) the zoanthid Palythoa caribaeorum and were compared to the water microbes collected 3 m above the reef. Microbial genera and functional potential were annotated using MG-RAST and showed that the dominant benthic macro-organisms influence the taxa and functions of microbes in the water column surrounding them, developing a specific “aura-biome”. The coral aura-biome reflected the open water column, and was associated with Synechococcus and functions suggesting oligotrophic growth, while the fleshy macroalgae aura-biome was associated with Ruegeria, Pseudomonas, and microbial functions suggesting low oxygen conditions. The turf algae aura-biome was associated with Vibrio, Flavobacterium, and functions suggesting pathogenic activity, while zoanthids were associated with Alteromonas and functions suggesting a stressful environment. Because each benthic organism has a distinct aura-biome, a change in benthic cover will change the microbial community of the water, which may lead to either the stimulation or suppression of the recruitment of benthic organisms.

Highlights

  • Coral reef ecosystems are diverse but declining habitats (Jackson & Buss, 1975; Hixon & Beets, 1993; Cantera et al, 2003; Hughes et al, 2010)

  • We propose that each benthic organism influences the microbiome in the water column boundary layers, promoting a benthic organism-specific microbial community that we call the ‘aura-biome’

  • Coral had a mean cover of 78.3 ± 2.9%, fleshy macroalgae had a mean cover of 93.8 ± 2.3%, turf algae had a mean cover of 83.3 ± 3.3%, and zoanthid had a mean cover of 88.3 ± 5.0% on the benthos

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Summary

Introduction

Coral reef ecosystems are diverse but declining habitats (Jackson & Buss, 1975; Hixon & Beets, 1993; Cantera et al, 2003; Hughes et al, 2010). Microbes associated with the water of pristine coral reefs show a mix of autotrophs and heterotrophs, while the water of degraded reefs is dominated by microbial heterotrophs including many pathogenic strains (Dinsdale et al, 2008a; Morrow et al, 2012). The increase of pathogenic microbes in the reef water column is correlated with an increase in the amount of coral disease (Dinsdale et al, 2008a). There are several hypotheses explaining the increase of pathogens on coral reefs; the first is that microbes are transported from agricultural and human sewage runoff into the ocean, and the second is that the microbial changes are being generated on the reef (Dinsdale & Rohwer, 2011)

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