Genomic analysis reveals versatile heterotrophic capacity of a potentially symbiotic sulfur‐oxidizing bacterium in sponge

Abstract

Sulfur-reducing bacteria (SRB) and sulfur-oxidizing bacteria (SOB) play essential roles in marine sponges. However, the detailed characteristics and physiology of the bacteria are largely unknown. Here, we present and analyse the first genome of sponge-associated SOB using a recently developed metagenomic binning strategy. The loss of transposase and virulence-associated genes and the maintenance of the ancient polyphosphate glucokinase gene suggested a stabilized SOB genome that might have coevolved with the ancient host during establishment of their association. Exclusive distribution in sponge, bacterial detoxification for the host (sulfide oxidation) and the enrichment for symbiotic characteristics (genes-encoding ankyrin) in the SOB genome supported the bacterial role as an intercellular symbiont. Despite possessing complete autotrophic sulfur oxidation pathways, the bacterium developed a much more versatile capacity for carbohydrate uptake and metabolism, in comparison with its closest relatives (Thioalkalivibrio) and to other representative autotrophs from the same order (Chromatiales). The ability to perform both autotrophic and heterotrophic metabolism likely results from the unstable supply of reduced sulfur in the sponge and is considered critical for the sponge-SOB consortium. Our study provides insights into SOB of sponge-specific clade with thioautotrophic and versatile heterotrophic metabolism relevant to its roles in the micro-environment of the sponge body.

Draft Genomes Shed Light on the Dual Bacterial Symbiosis that Dominates the Microbiome of the Coral Reef Sponge Amphimedon queenslandica

“…These all clade with different representatives of Alphaproteobacteria, and specifically within the orders Rhodobacterales and the Rhodospirilales. This same association was also discussed by Tian et al (2014) for T. sp. HK1 (Figure 4C).…”

“…Sulfur-oxidizing symbionts have varied metabolic capabilities, with some displaying obligate autotrophy while others can grow heterotrophically or mixotrophically (Kleiner et al, 2012a;Tian et al, 2014). We find no evidence for a complete carbon fixation mechanism in AqS1, although we acknowledge that this could be due to limitations of our current draft genome assembly.…”

“…Heterotrophy in general has been reported in several other sponge symbionts Siegl et al, 2011;Fan et al, 2012;Bondarev et al, 2013;Tian et al, 2014). Interestingly, a large proportion of genes that endow the AqS1 symbiont with heterotrophic capabilities are most closely related to genes of several alphaproteobacteria.…”

“…The partial sequence from T. sp. HK1 reported in Tian et al (2014) was kindly provided by Dr Ren-Mao Tian. A sequence alignment was derived with PyNAST (Caporaso et al, 2010a) using the template file "core_set_aligned.fasta.imputed" from QIIME v. 1.8.0 (Caporaso et al, 2010b) and manually checked using AliView (Larsson, 2014).…”

“…Single-cell genomic and metagenomics studies have contributed to correlating particular traits with specific symbiont lineages Siegl et al, 2011;Kamke et al, 2013;Gao et al, 2014;Tian et al, 2014;Wilson et al, 2014;Burgsdorf et al, 2015;Britstein et al, 2016), revealing functional gene convergence in phylogenetically-distinct microbial communities with core features that likely reflect adaptation of microorganisms to the sponge host environment Hentschel et al, 2012). Traits that have repeatedly been reported in prokaryote symbionts of poriferans include versatile nutrient utilization, protection from environmental and host-specific stress, and eukaryotic-like proteins Hentschel et al, 2012).…”