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Genome-Scale Analysis of Acetobacterium Bakii Reveals the Cold Adaptation of Psychrotolerant Acetogens by Post-Transcriptional Regulation

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Genome-Scale Analysis of Acetobacterium Bakii Reveals the Cold Adaptation of Psychrotolerant Acetogens by Post-Transcriptional Regulation Downloaded from rnajournal.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Shin et al. 1 Genome-scale analysis of Acetobacterium bakii reveals the cold adaptation of 2 psychrotolerant acetogens by post-transcriptional regulation 3 4 Jongoh Shin1, Yoseb Song1, Sangrak Jin1, Jung-Kul Lee2, Dong Rip Kim3, Sun Chang Kim1,4, 5 Suhyung Cho1*, and Byung-Kwan Cho1,4* 6 7 1Department of Biological Sciences and KI for the BioCentury, Korea Advanced Institute of 8 Science and Technology, Daejeon 34141, Republic of Korea 9 2Department of Chemical Engineering, Konkuk University, Seoul 05029, Republic of Korea 10 3Department of Mechanical Engineering, Hanyang University, Seoul 04763, Republic of Korea 11 4Intelligent Synthetic Biology Center, Daejeon 34141, Republic of Korea 12 13 *Correspondence and requests for materials should be addressed to S.C. ([email protected]) 14 and B.-K.C. ([email protected]) 15 16 Running title: Cold adaptation of psychrotolerant acetogen 17 18 Keywords: Post-transcriptional regulation, Psychrotolerant acetogen, Acetobacterium bakii, 19 Cold-adaptive acetogenesis 20 1 Downloaded from rnajournal.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Shin et al. 1 ABSTRACT 2 Acetogens synthesize acetyl-CoA via CO2 or CO fixation, producing organic compounds. 3 Despite their ecological and industrial importance, their transcriptional and post-transcriptional 4 regulation has not been systematically studied. With completion of the genome sequence of 5 Acetobacterium bakii (4.28-Mb), we measured changes in the transcriptome of this 6 psychrotolerant acetogen in response to temperature variations under autotrophic and 7 heterotrophic growth conditions. Unexpectedly, acetogenesis genes were highly upregulated at 8 low temperatures under heterotrophic, as well as autotrophic, growth conditions. To 9 mechanistically understand the transcriptional regulation of acetogenesis genes via changes in 10 RNA secondary structures of 5′-untranslated regions (5′-UTR), the primary transcriptome was 11 experimentally determined, and 1,379 transcription start sites (TSS) and 1,100 5′-UTR were 12 found. Interestingly, acetogenesis genes contained longer 5′-UTR with lower RNA-folding free 13 energy than other genes, revealing that the 5′-UTRs control the RNA abundance of the 14 acetogenesis genes under low temperature conditions. Our findings suggest that post- 15 transcriptional regulation via RNA conformational changes of 5′-UTRs is necessary for cold- 16 adaptive acetogenesis. 17 18 INTRODUCTION 19 Microbial conversion of single carbon (C1) compounds, such as CO and CO2, to biofuels and 20 commodity chemicals, has been considered as one of the sustainable routes for the replacement 21 of fossil resources (Henstra et al. 2007; Bengelsdorf et al. 2013; Latif et al. 2014). In particular, 22 acetogens are attractive biocatalysts, since they can grow autotrophically with CO2 as the sole 23 carbon source and H2 as the electron donor, producing acetate as a primary end product (Drake 2 Downloaded from rnajournal.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Shin et al. 1 1995). This unique metabolism in acetogens is mediated by the reductive acetyl-CoA pathway 2 referred to as the Wood-Ljungdahl pathway (WLP), which provides a highly efficient system for 3 converting CO and CO2 to various biochemicals including acetate, ethanol, 2,3-butanediol, 4 butyrate, and butanol (Schiel-Bengelsdorf and Dürre 2012). 5 Acetogens are physiologically defined as a group of anaerobic bacteria that synthesize 6 acetyl-CoA as a central metabolic intermediate from chemolithoautotrophic substrates (Drake 7 1995). Acetogens comprise at least 23 different genera (Drake et al. 2006) and their growth 8 environments range from anoxic freshwater, soils, marine sediments, and sewage sludge to the 9 gastrointestinal tracts of insects and animals (Drake et al. 2006). Thus, systematic understanding 10 of their genetic backgrounds, as well as of transcriptional and translational regulation in response 11 to environmental factors, is a prerequisite for the full exploitation of their biosynthetic potential. 12 One example is the anaerobic growth of acetogens at low temperatures, of particular interest in 13 view of its ecological significance (Nozhevnikova et al. 1994). Several cold-active acetogens 14 were isolated from cold environments (Nozhevnikova et al. 1994; Kotsyurbenko et al. 1995; 15 Simankova et al. 2000; Kotsyurbenko et al. 2001; Nozhevnikova et al. 2001) including 16 perennially ice-covered sediments (Sattley and Madigan 2007). They are all affiliated with the 17 genus Acetobacterium, reflecting their phylogenetic proximity. The isolated bacteria are all 18 psychrotolerant and proliferate at temperatures as low as 1 ºC. Although both mesophilic and 19 thermophilic acetogens have been extensively studied, the mechanisms of cold adaptation and 20 the regulation of acetogenesis, including the WLP and the energy conservation systems of 21 psychrotolerant acetogens, remain elusive. 22 In transcriptional and post-transcriptional regulation, DNA sequences such as principal 23 promoter elements and 5′-untranslated regions (5′-UTRs) play a critical role as genome- 3 Downloaded from rnajournal.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Shin et al. 1 embedded cis-acting determinants (Jeong et al. 2016). The identification of transcription start 2 sites (TSSs) via differential RNA sequencing (dRNA-Seq) has facilitated the definition of 3 bacterial operons and regulatory sequences (Sharma et al. 2010; Sharma and Vogel 2014). The 4 latter approach, combined with RNA sequencing (RNA-Seq) for the study of gene expression, 5 now allows for quantitative analysis of transcriptional and translational regulation in various 6 species with unprecedented detail (Sharma and Vogel 2014; Jeong et al. 2017). Also, the precise 7 mapping of TSSs enables to define the sequence and structure of the mRNA 5′ ends, thus 8 providing insights into mRNA stability and translational efficiency (Jeong et al. 2016). Thus, we 9 describe a systematic approach toward the integration of genome, primary transcriptome, and 10 transcriptome data from a psychrotolerant acetogen, Acetobacterium bakii DSM 8239, originally 11 isolated from a cold environment (< 6 ºC) (Kotsyurbenko et al. 1995) and displaying a higher 12 growth rate at 1 °C than Acetobacterium paludosum and Acetobacterium fimetarium 13 (Kotsyurbenko et al. 1995). We completed the A. bakii genome sequence and identified unique 14 expression patterns of acetogenesis genes under optimal and low temperature growth conditions. 15 We also determined the genome-wide location of TSSs to investigate the role of cis-acting 16 elements including 5′-UTRs, promoter elements, and Shine-Dalgarno (SD) sequences. Our data 17 suggest that the RNA regulatory elements embedded in the 5′-UTR orchestrate the gene 18 expression changes underlying adaptation to a cold environment. 19 20 RESULTS 21 Completion of the genome sequence of the psychrotolerant bacterium A. bakii 22 To complete the A. bakii genome sequence, we employed single-molecule real-time (SMRT) 23 sequencing, yielding 108,817 quality-trimmed long reads (6,297 bp of average length). The 4 Downloaded from rnajournal.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Shin et al. 1 genome was assembled using a hierarchical genome assembly process (HGAP v2.3.0), the 2 SSPACE scaffolding algorithm (Hunt et al. 2014) with Illumina mate-pair sequencing data, and a 3 PCR-based primer walking method. The genome was polished using two types of short high- 4 fidelity sequence reads obtained from whole genome paired-end sequencing and strand-specific 5 RNA sequencing (RNA-Seq). One scaffold (4.28-Mb) and one short contig (35-kb) were finally 6 assembled as a chromosome and a plasmid DNA, respectively (Supplemental Table S1). 7 However, the 35-kb contig could not be assembled as a circular DNA, suggesting that it was an 8 unfinished product resulting from incomplete assembly. A total of 112 nucleotide conflicts 9 between Illumina short read sequences and the assembled genome sequence were corrected by 10 the Illumina short read sequences (Supplemental Table S2). The 4.28-Mb genome, with a GC 11 content of 41.3%, was annotated for 3,973 coding genes (CDS), 22 ribosomal RNAs (rRNA), 12 and 69 transfer RNAs (tRNA) genes. Compared to the previous draft genome sequence (Hwang 13 et al. 2015), an additional 183,963 bps and 280 genes were identified including large repeats and 14 structural variations, such as rRNA genes (Supplemental Table S1). Importantly, the methyl- 15 branch of the WLP, including a formyl-tetrahydrofolate (THF) synthetase (ABAKI_c24790) and 16 a V-type ATP synthase gene cluster (ABAKI_c03210 – ABAKI_c03290), were newly uncovered 17 in the completed genome. 18 The genomes of several model acetogens, such as Acetobacterium woodii (Poehlein et al. 19 2012), Clostridium ljungdahlii (Köpke et al. 2010), Clostridium autoethanogenum (Brown et al. 20 2014), and Moorella thermoacetica (Pierce et al. 2008), have been reported. Despite their genetic 21 diversity, acetogens share highly conserved gene clusters for autotrophic growth, such as the 22 WLP, central metabolic pathways, and cofactor biosynthetic pathways (Poehlein et al. 2015; 23 Shin et al. 2016). Pairwise genome comparison showed that A. bakii was most closely related to 5 Downloaded
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