Abstract

Black Band Disease (BBD), the destructive microbial consortium dominated by the cyanobacterium Roseofilum reptotaenium, affects corals worldwide. While the taxonomic composition of BBD consortia has been well-characterized, substantially less is known about its functional repertoire. We sequenced the metagenomes of Caribbean and Pacific black band mats and cultured Roseofilum and obtained five metagenome-assembled genomes (MAGs) of Roseofilum, nine of Proteobacteria, and 12 of Bacteroidetes. Genomic content analysis suggests that Roseofilum is a source of organic carbon and nitrogen, as well as natural products that may influence interactions between microbes. Proteobacteria and Bacteroidetes members of the disease consortium are suited to the degradation of amino acids, proteins, and carbohydrates. The accumulation of sulfide underneath the black band mat, in part due to a lack of sulfur oxidizers, contributes to the lethality of the disease. The presence of sulfide:quinone oxidoreductase genes in all five Roseofilum MAGs and in the MAGs of several heterotrophs demonstrates that resistance to sulfide is an important characteristic for members of the BBD consortium.

Highlights

  • Black Band Disease (BBD) is a globally distributed coral disease that devastates dozens of species of corals, including large, reef-building scleractinians (Sato et al, 2016)

  • BBD consortia resemble microbial mats found in tropical lagoons (Echenique-Subiabre et al, 2015), mangroves (Guidi-Rotani et al, 2014), and modern marine stromatolites (Ruvindy et al, 2016) that are characterized by steep physicochemical gradients and the presence of Cyanobacteria, Bacteroidetes, and Proteobacteria

  • To uncover the mechanisms through which Roseofilum proliferates and engineers a new environment on the surface of corals during BBD, we examined the metagenomic potential of members of black band consortia in situ and in vitro

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Summary

INTRODUCTION

Black Band Disease (BBD) is a globally distributed coral disease that devastates dozens of species of corals, including large, reef-building scleractinians (Sato et al, 2016). Strains of Roseofilum have been cultivated in the laboratory, but like other filamentous cyanobacteria, Roseofilum cannot be fully isolated, only grown in non-axenic, unicyanobacterial cultures (Richardson et al, 2014) This conserved interdependence of Roseofilum and heterotrophic bacteria may be linked to metabolic requirements and may explain why this cyanobacterium is found within apparently healthy coral microbiomes (Meyer et al, 2016). Roseofilum is a rare but ubiquitous member of healthy Caribbean coral microbiota, implying that growth of Roseofilum is constrained in healthy tissue until undefined restrictions are removed (Meyer et al, 2016) Together, this suggests that while Roseofilum is capable of engineering the highly altered black band layer, its influence is spatially limited and its pathogenesis is contextual. To uncover the mechanisms through which Roseofilum proliferates and engineers a new environment on the surface of corals during BBD, we examined the metagenomic potential of members of black band consortia in situ and in vitro

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