Unraveling the microbial processes of black band disease in corals through integrated genomics

Thomas Rattei,Bette L. Willis,Patrick Laffy,Yui Sato,David G. Bourne,Karen D. Weynberg,Dmitrij Turaev,Edmund Y. S. Ling

doi:10.1038/srep40455

Abstract

Coral disease outbreaks contribute to the ongoing degradation of reef ecosystems, however, microbial mechanisms underlying the onset and progression of most coral diseases are poorly understood. Black band disease (BBD) manifests as a cyanobacterial-dominated microbial mat that destroys coral tissues as it rapidly spreads over coral colonies. To elucidate BBD pathogenesis, we apply a comparative metagenomic and metatranscriptomic approach to identify taxonomic and functional changes within microbial lesions during in-situ development of BBD from a comparatively benign stage termed cyanobacterial patches. Results suggest that photosynthetic CO2-fixation in Cyanobacteria substantially enhances productivity of organic matter within the lesion during disease development. Photosynthates appear to subsequently promote sulfide-production by Deltaproteobacteria, facilitating the major virulence factor of BBD. Interestingly, our metagenome-enabled transcriptomic analysis reveals that BBD-associated cyanobacteria have a putative mechanism that enables them to adapt to higher levels of hydrogen sulfide within lesions, underpinning the pivotal roles of the dominant cyanobacterium within the polymicrobial lesions during the onset of BBD. The current study presents sequence-based evidence derived from whole microbial communities that unravel the mechanism of development and progression of BBD.

Highlights

Changes in microbial communities during the development of BBD from CP have been extensively investigated and documented as a model study system of BBD pathogenesis[10]
Key changes during the development of BBD from CP include (1) an increase in the overall virulence of the lesion, as measured by progression rates on coral tissue[11], (2) a shift in the dominant cyanobacterium to a phylogenetically distinct species[11], (3) increased relative proportions of sulfide-reducing bacteria (SRB) and decreased relative abundance of sulfide-oxidizing bacteria (SOB)[12,13], (4) a shift in the archaeal community composition to a community dominated by a novel archaeal species[14], and (5) the formation of anoxic and sulfide-rich microenvironmental conditions within BBD lesions, with diurnal dynamics, that are correlated to the overall virulence[15]
In both metagenomes and metatranscriptomes, the majority of CP-derived taxonomic marker genes were affiliated to Cyanobacteria, Proteobacteria and Bacteroidetes; BBD-derived taxonomic marker sequences were dominated by sequences associated with Cyanobacteria and Proteobacteria, but the Bacteroidetes did not represent a major component of BBD communities (Fig. 2a; see Supplementary document for detailed comparisons of sequences taxonomically associated with Bacteria, as well as information on eukaryotic, archaeal and viral-associated sequences)

Summary

Introduction

Changes in microbial communities during the development of BBD from CP have been extensively investigated and documented as a model study system of BBD pathogenesis[10]. What triggers CP remains to be investigated, the discovery of these changes during the transition from CP to BBD represented an important step towards a mechanistic understanding of BBD pathogenesis. Findings from the CP-BBD system have been synthesized into a conceptual model to illustrate the development of BBD pathogenicity[10], a detailed understanding of microbial drivers contributing to the development of virulence have not been achieved due to the lack of investigations into the functions of microbial members and their interactions at a whole lesion community scale. The microbial community structure and functional properties were directly compared between CP and BBD to identify the mechanisms playing central roles in the development of increased virulence specific to the BBD lesion

Methods

Results

Conclusion