Potential syntrophic relationship between coral-associated Prosthecochloris and its companion sulfate-reducing bacterium unveiled by genomic analysis

Abstract

Endolithic microbial symbionts in the coral skeleton may play a pivotal role in maintaining coral health. However, compared to aerobic micro-organisms, research on the roles of endolithic anaerobic micro-organisms and microbe–microbe interactions in the coral skeleton are still in their infancy. In our previous study, we showed that a group of coral-associated Prosthecochloris (CAP), a genus of anaerobic green sulphur bacteria, was dominant in the skeleton of the coral Isopora palifera. Though CAP is diverse, the 16S rRNA phylogeny presents it as a distinct clade separate from other free-living Prosthecochloris . In this study, we build on previous research and further characterize the genomic and metabolic traits of CAP by recovering two new high-quality CAP genomes – Candidatus Prosthecochloris isoporae and Candidatus Prosthecochloris sp. N1 – from the coral I. palifera endolithic cultures. Genomic analysis revealed that these two CAP genomes have high genomic similarities compared with other Prosthecochloris and harbour several CAP-unique genes. Interestingly, different CAP species harbour various pigment synthesis and sulphur metabolism genes, indicating that individual CAPs can adapt to a diversity of coral microenvironments. A novel high-quality genome of sulfate-reducing bacterium (SRB)– Candidatus Halodesulfovibrio lyudaonia – was also recovered from the same culture. The fact that CAP and various SRB co-exist in coral endolithic cultures and coral skeleton highlights the importance of SRB in the coral endolithic community. Based on functional genomic analysis of Ca. P. sp. N1, Ca. P. isoporae and Ca. H. lyudaonia, we also propose a syntrophic relationship between the SRB and CAP in the coral skeleton.

Microbial bioindicators of Stony Coral Tissue Loss Disease identified in corals and overlying waters using a rapid field‐based sequencing approach

“…Alternatively, the syringe‐based collection method results in a homogenate of newly compromised, diseased tissue, as well as necrotic or sloughed off tissue that likely captures potential pathogen(s), organisms involved in secondary infections, or even saprophytic microorganisms proliferating off the exposed skeleton and dead coral tissue (Burge et al ., 2013; Egan and Gardiner, 2016). For example, the finding of increased Deltaproteobacteria in diseased samples of M. cavernosa and the significant enrichment of Halodesulfovibrio , known sulfate‐reducing bacteria, may have been a signature of the exposed coral skeleton (Chen et al ., 2021), or perhaps anaerobic degradation of coral tissue (Viehman et al ., 2006). Overall, the finding that disease impacts coral microbiome structure in the USVI is supported by previous findings that show shifts in coral microbiomes between healthy and diseased corals in Florida, USA (Meyer et al ., 2019; Rosales et al ., 2020).…”

Genomic view of the diversity and functional role of archaea and bacteria in the skeleton of the reef-building corals Porites lutea and Isopora palifera

“…Sulfate reducers, including Desulfobacteria , were first reported in the skeleton of Goniastrea aspera [ 101 ], but genes related to sulfur reduction were first identified in healthy and yellow bands of coral Orbicella faveolata [ 11 ]. Recently, metagenomic analysis of the skeleton of coral I. palifera and subsequent culturing and genomic analysis of dominant green sulfur bacteria (GSB) proposed a potential syntrophic relationship between GSB and SRB, where GSB can provide sulfate, which is used by SRB as an electron acceptor to generate biogenic H 2 S, which in turn is used by GSB as an electron donor [ 20 , 103 ]. In this study, MAGs belonging to the genus Chlorobium (class: Chlorobia ) and Desulfobacter (class: Desulfobacteria ) were recovered from the skeleton of P. lutea , indicating the possibility of a similar syntrophic relationship in the skeleton (Fig.…”

How does heat stress affect sponge microbiomes? Structure and resilience of microbial communities of marine sponges from different habitats

“…Apart from genus Fusibacter and family Marinifilaceae, the microbiome of heat stressed A. oroides was enriched in family Clostridiaceae, order Peptostreptococcales-Tissierellales, and genera Halodesulfovibio. Genus Halodesulfovibrio has been found in corals and species from this genus seem to have antimicrobial properties (Shivani et al, 2017;Chen et al, 2021). Despite all the differences observed between studies it must be noted that observed differences may be influenced by the use of different methodologies, e.g.…”