Transcriptomic and proteomic insight into the mechanism of cyclooctasulfur‐ versus thiosulfate‐oxidation by the chemolithoautotroph Sulfurimonas denitrificans

Abstract

Summary Chemoautotrophic bacteria belonging to the genus Sulfurimonas (class Campylobacteria) were previously identified as key players in the turnover of zero‐valence sulfur, a central intermediate in the marine sulfur cycle. S. denitrificans was further shown to be able to oxidize cyclooctasulfur (S8). However, at present the mechanism of activation and metabolism of cyclooctasulfur is not known. Here, we assessed the transcriptome and proteome of S. denitrificans grown with either thiosulfate or S8 as the electron donor. While the overall expression profiles under the two growth conditions were rather similar, distinct differences were observed that could be attributed to the utilization of S8. This included a higher abundance of expressed genes related to surface attachment in the presence of S8, and the differential regulation of the sulfur‐oxidation multienzyme complex (SOX), which in S. denitrificans is encoded in two gene clusters: soxABXY 1Z 1 and soxCDY 2Z 2. While the proteins of both clusters were present with thiosulfate, only proteins of the soxCDY 2Z 2 were detected at significant levels with S8. Based on these findings a model for the oxidation of S8 is proposed. Our results have implications for interpreting metatranscriptomic and ‐proteomic data and for the observed high level of diversification of soxY 2Z 2 among sulfur‐oxidizing Campylobacteria.

Comparison of sulfide‐oxidizing Sulfurimonas strains reveals a new mode of thiosulfate formation in subsurface environments

“…B). While growth rates were not explicitly determined in this study, doubling times have been reported as 1.3 h for strain CVO growing with sulfide and nitrate (Gevertz et al ., ), and 8 and 11 h for S. denitrificans growing with either thiosulfate or S 8 (Götz et al ., ). Growth was tracked in the present study based on the measurement of total RNA over the time course of the experiments (Fig.…”

“…In all Sulfurimonas genomes, the soxCDY 2 Z 2 genes are located adjacent to a gene annotated as putative metallo hydrolase (protein superfamily SSF56281) that bears some similarity to the soxH gene of P. pantotrophus (23% protein sequence identity), that was annotated as a thiol hydrolase (Friedrich et al ., ; Götz et al ., ). While S. denitrificans showed high expression of the soxCDY 2 Z 2 H cluster during oxidation of sulfide and S 0 (Fig.…”

“…We compared the genome and transcriptome of strain CVO with the closely related S. denitrificans DSM 1251 under the same growth conditions to detect genotypic and metabolic differences. Our findings confirmed a newly proposed role of the sox gene products in S 0 oxidation (Götz et al ., ) and reveal a new and likely widespread mechanism for thiosulfate formation. In addition, we provide evidence for different modes by which Sulfurimonas spp.…”

“…The organization of separate sox gene clusters in Sulfurimonas spp. may indicate a loss of co‐dependency of the individual genes for oxidation of certain sulfur compounds; indeed, both gene clusters appear to be differentially regulated in Sulfurimonas denitrificans DSM 1251 when growing on zero‐valent cyclooctasulfur (S 8 ) compared with thiosulfate (Götz et al ., ).…”

Transcriptomic response ofNitrosomonas europaeatransitioned from ammonia- to oxygen-limited steady-state growth

“…To test for statistically significant differences between transcriptomes obtained from NH 3 - and O 2 -limited steady-state growth, TPMs of biological triplicate samples were used to calculate p-values based on a Welch’s t-test. The more stringent Welch’s, rather than the Student’s t-Test was selected due to the limited number of biological replicates (57). Additionally, linear fold changes between average TPMs under both growth conditions for each expressed ORF were calculated.…”