Abstract

Calderihabitans maritimus KKC1 is a thermophilic, carbon monoxide (CO)-utilizing, hydrogen-evolving bacterium that harbors seven cooS genes for anaerobic CO dehydrogenases and six hyd genes for [NiFe] hydrogenases and capable of using a variety of electron acceptors coupled to CO oxidation. To understand the relationships among these unique features and the transcriptional adaptation of the organism to CO, we performed a transcriptome analysis of C. maritimus KKC1 grown under 100% CO and N2 conditions. Of its 3114 genes, 58 and 32 genes were significantly upregulated and downregulated in the presence of CO, respectively. A cooS–ech gene cluster, an “orphan” cooS gene, and bidirectional hyd genes were upregulated under CO, whereas hydrogen-uptake hyd genes were downregulated. Transcriptional changes in anaerobic respiratory genes supported the broad usage of electron acceptors in C. maritimus KKC1 under CO metabolism. Overall, the majority of the differentially expressed genes were oxidoreductase-like genes, suggesting metabolic adaptation to the cellular redox change upon CO oxidation. Moreover, our results suggest a transcriptional response mechanism to CO that involves multiple transcription factors, as well as a CO-responsive transcriptional activator (CooA). Our findings shed light on the diverse mechanisms for transcriptional and metabolic adaptations to CO in CO-utilizing and hydrogen-evolving bacteria.

Highlights

  • Carbon monoxide (CO) is used as an energy source by carbon monoxide (CO)-oxidizing microbes because of its low redox potential (Ragsdale 2004; Oelgeschläger and Rother 2008; Sokolova et al 2009; Diender et al.1 3 Vol.:(0123456789)Extremophiles (2020) 24:551–5642015)

  • We performed RNA sequencing (RNA-seq) experiments for late-exponential cultures of C. maritimus KKC1 grown under 100% CO and ­N2 gas conditions in biological duplicates (Fig. 1a)

  • 60% of the upregulated and ~ 70% of the downregulated Differentially expressed genes (DEGs) in the presence of CO were grouped into the “metabolism” categories of Clusters of Orthologous Groups (COGs) (Galperin et al 2015), with > 40% of both upregulated and downregulated DEGs were grouped in the COG functional category “C” (Table S2)

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Summary

Introduction

Carbon monoxide (CO) is used as an energy source by CO-oxidizing microbes (carboxydotrophs) because of its low redox potential (Ragsdale 2004; Oelgeschläger and Rother 2008; Sokolova et al 2009; Diender et al. Vol.:(0123456789)Extremophiles (2020) 24:551–5642015). Unlike aerobic CODHs, NiCODHs can reduce ferredoxin and thereby utilize various types of terminal electron acceptors, such as protons, ­CO2, sulfate, and ferric iron [Fe(III)] (Oelgeschläger and Rother 2008; Sokolova et al 2009; Diender et al 2015). Because of this unique feature of Ni-CODHs, physiologically diverse anaerobic carboxydotrophs have been described, such as hydrogenogens, acetogens, methanogens, sulfate reducers, and Fe(III) reducers (Oelgeschläger and Rother 2008; Sokolova et al 2009; Diender et al 2015)

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