Genome-scale analysis of Acetobacterium bakii reveals the cold adaptation of psychrotolerant acetogens by post-transcriptional regulation.

Jongoh Shin,Sangrak Jin,Yoseb Song,Jung-Kul Lee,Dong Rip Kim,Suhyung Cho,Sun Chang Kim,Byung-Kwan Cho

doi:10.1261/rna.068239.118

Abstract

Acetogens synthesize acetyl-CoA via CO2 or CO fixation, producing organic compounds. Despite their ecological and industrial importance, their transcriptional and post-transcriptional regulation has not been systematically studied. With completion of the genome sequence of Acetobacterium bakii (4.28-Mb), we measured changes in the transcriptome of this psychrotolerant acetogen in response to temperature variations under autotrophic and heterotrophic growth conditions. Unexpectedly, acetogenesis genes were highly up-regulated at low temperatures under heterotrophic, as well as autotrophic, growth conditions. To mechanistically understand the transcriptional regulation of acetogenesis genes via changes in RNA secondary structures of 5′-untranslated regions (5′-UTR), the primary transcriptome was experimentally determined, and 1379 transcription start sites (TSS) and 1100 5′-UTR were found. Interestingly, acetogenesis genes contained longer 5′-UTR with lower RNA-folding free energy than other genes, revealing that the 5′-UTRs control the RNA abundance of the acetogenesis genes under low temperature conditions. Our findings suggest that post-transcriptional regulation via RNA conformational changes of 5′-UTRs is necessary for cold-adaptive acetogenesis.

Highlights

Microbial conversion of single carbon (C1) compounds, such as CO and CO2, to biofuels and commodity chemicals, has been considered as one of the sustainable routes for the replacement of fossil resources (Henstra et al 2007; Bengelsdorf et al 2013; Latif et al 2014)
Hierarchical clustering and principal component analysis regulation of the lactate dehydrogenase (LDH) operon previously reported for A. woodii (Weghoff et al 2015), we found that the gene expression of the LDH gene in the C1 cluster was repressed under heterotrophic growth conditions (Fig. 4C)
We completed the genome sequence of the psychrotolerant acetogen Acetobacterium bakii DSM 8239 (4.28 Mbp in size) and revealed transcriptomes associated to autotrophic growth at low temperature

Summary

Introduction

Microbial conversion of single carbon (C1) compounds, such as CO and CO2, to biofuels and commodity chemicals, has been considered as one of the sustainable routes for the replacement of fossil resources (Henstra et al 2007; Bengelsdorf et al 2013; Latif et al 2014). Acetogens are attractive biocatalysts, since they can grow autotrophically with CO2 as the sole carbon source and H2 as the electron donor, producing acetate as a primary end product (Drake 1995). This unique metabolism in acetogens is mediated by the reductive acetyl-CoA pathway referred to as the Wood–Ljungdahl pathway (WLP), which provides a highly efficient system for converting CO and CO2 to various biochemicals including acetate, ethanol, 2,3-butanediol, butyrate, and butanol (Schiel-Bengelsdorf and Dürre 2012). One example is the anaerobic growth of acetogens at low temperatures, of particular interest in view of its ecological significance (Nozhevnikova et al 1994). Several cold-active acetogens were isolated from cold environments (Nozhevnikova et al 1994, 2001; Kotsyurbenko et al 1995, 2001; Simankova et al 2000) including perennially ice-covered sediments

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Conclusion