Single-Cell Genomics of Novel Actinobacteria With the Wood–Ljungdahl Pathway Discovered in a Serpentinizing System

Merino, Nancy; Kawai, Mikihiko; Boyd, Eric S.; Colman, Daniel R.; McGlynn, Shawn E.; Nealson, Kenneth H.; Kurokawa, Ken; Hongoh, Yuichi

doi:10.3389/fmicb.2020.01031

Title: Single-Cell Genomics of Novel Actinobacteria With the Wood–Ljungdahl Pathway Discovered in a Serpentinizing System

Journal Article · Tue Jun 09 00:00:00 EDT 2020 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2020.01031· OSTI ID:1633526

Merino, Nancy ^[1]; Kawai, Mikihiko ^[2]; Boyd, Eric S. ^[3]; Colman, Daniel R. ^[3]; McGlynn, Shawn E. ^[4]; Nealson, Kenneth H. ^[5]; Kurokawa, Ken ^[6]; Hongoh, Yuichi ^[7]

Tokyo Institute of Technology (Japan); Univ. of Southern California, Los Angeles, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Kyoto Univ. (Japan); Tokyo Institute of Technology (Japan)
Montana State Univ., Bozeman, MT (United States)
Tokyo Institute of Technology (Japan); Blue Marble Space Institute of Science, Seattle, WA (United States); RIKEN, Saitama (Japan)
Univ. of Southern California, Los Angeles, CA (United States)
Tokyo Institute of Technology (Japan); National Inst. of Genetics, Shizuoka (Japan)
Tokyo Institute of Technology (Japan)

Serpentinite-hosted systems represent modern-day analogs of early Earth environments. In these systems, water-rock interactions generate highly alkaline and reducing fluids that can contain hydrogen, methane, and low-molecular-weight hydrocarbons-potent reductants capable of fueling microbial metabolism. In this study, we investigated the microbiota of Hakuba Happo hot springs (~50°C; pH~10.5–11), located in Nagano (Japan), which are impacted by the serpentinization process. Analysis of the 16S rRNA gene amplicon sequences revealed that the bacterial community comprises Nitrospirae (47%), “Parcubacteria” (19%), Deinococcus-Thermus (16%), and Actinobacteria (9%), among others. Notably, only 57 amplicon sequence variants (ASV) were detected, and fifteen of these accounted for 90% of the amplicons. Among the abundant ASVs, an early-branching, uncultivated actinobacterial clade identified as RBG-16-55-12 in the SILVA database was detected. Ten single-cell genomes (average pairwise nucleotide identity: 0.98–1.00; estimated completeness: 33–93%; estimated genome size: ~2.3 Mb) that affiliated with this clade were obtained. Taxonomic classification using single copy genes indicates that the genomes belong to the actinobacterial class-level clade UBA1414 in the Genome Taxonomy Database. Based on metabolic pathway predictions, these actinobacteria are anaerobes, capable of glycolysis, dissimilatory nitrate reduction and CO₂ fixation via the Wood–Ljungdahl (WL) pathway. Several other genomes within UBA1414 and two related class-level clades also encode the WL pathway, which has not yet been reported for the Actinobacteria phylum. For the Hakuba actinobacterium, the energy metabolism related to the WL pathway is likely supported by a combination of the Rnf complex, group 3b and 3d [NiFe]-hydrogenases, [FeFe]-hydrogenases, and V-type (H⁺/Na⁺ pump) ATPase. The genomes also harbor a form IV ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO) complex, also known as a RubisCO-like protein, and contain signatures of interactions with viruses, including clustered regularly interspaced short palindromic repeat (CRISPR) regions and several phage integrases. This is the first report and detailed genome analysis of a bacterium within the Actinobacteria phylum capable of utilizing the WL pathway. The Hakuba actinobacterium is a member of the clade UBA1414/RBG-16-55-12, formerly within the group “OPB41.” We propose to name this bacterium ‘Candidatus Hakubanella thermoalkaliphilus.'

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1633526

Report Number(s):: LLNL-JRNL-800258; 1003505

Journal Information:: Frontiers in Microbiology, Vol. 11, Issue no. 11; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 18 works

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