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Carbon fixation pathways across the bacterial and archaeal tree of life.

ABSTRACT: Carbon fixation is a critical process for our planet; however, its distribution across the bacterial and archaeal domains of life has not been comprehensively studied. Here, we performed an analysis of 52,515 metagenome-assembled genomes and discover carbon fixation pathways in 1,007 bacteria and archaea. We reveal the genomic potential for carbon fixation through the reverse tricarboxylic acid cycle in previously unrecognized archaeal and bacterial phyla (i.e. Thermoplasmatota and Elusimicrobiota) and show that the 3-hydroxypropionate bi-cycle is not, as previously thought, restricted to the phylum Chloroflexota. The data also substantially expand the phylogenetic breadth for autotrophy through the dicarboxylate/4-hydroxybutyrate cycle and the Calvin-Benson-Bassham cycle. Finally, the genomic potential for carbon fixation through the 3-hydroxypropionate/4-hydroxybutyrate cycle, previously exclusively found in Archaea, was also detected in the Bacteria. Carbon fixation thus appears to be much more widespread than previously known, and this study lays the foundation to better understand the role of archaea and bacteria in global primary production and how they contribute to microbial carbon sinks.

SUBMITTER: Garritano AN

PROVIDER: S-EPMC9802188 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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Carbon fixation pathways across the bacterial and archaeal tree of life.

Garritano Alessandro N AN Song Weizhi W Thomas Torsten T

PNAS nexus 20221004 5

Carbon fixation is a critical process for our planet; however, its distribution across the bacterial and archaeal domains of life has not been comprehensively studied. Here, we performed an analysis of 52,515 metagenome-assembled genomes and discover carbon fixation pathways in 1,007 bacteria and archaea. We reveal the genomic potential for carbon fixation through the reverse tricarboxylic acid cycle in previously unrecognized archaeal and bacterial phyla (i.e. <i>Thermoplasmatota</i> and <i>Elu ...[more]

PMID: 36712370

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Project description:BackgroundAcidithiobacillus ferrooxidans is chemolithoautotrophic γ-proteobacterium that thrives at extremely low pH (pH 1-2). Although a substantial amount of information is available regarding CO2 uptake and fixation in a variety of facultative autotrophs, less is known about the processes in obligate autotrophs, especially those living in extremely acidic conditions, prompting the present study.ResultsFour gene clusters (termed cbb1-4) in the A. ferrooxidans genome are predicted to encode enzymes and structural proteins involved in carbon assimilation via the Calvin-Benson-Bassham (CBB) cycle including form I of ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO, EC 4.1.1.39) and the CO2-concentrating carboxysomes. RT-PCR experiments demonstrated that each gene cluster is a single transcriptional unit and thus is an operon. Operon cbb1 is divergently transcribed from a gene, cbbR, encoding the LysR-type transcriptional regulator CbbR that has been shown in many organisms to regulate the expression of RubisCO genes. Sigma70-like -10 and -35 promoter boxes and potential CbbR-binding sites (T-N11-A/TNA-N7TNA) were predicted in the upstream regions of the four operons. Electrophoretic mobility shift assays (EMSAs) confirmed that purified CbbR is able to bind to the upstream regions of the cbb1, cbb2 and cbb3 operons, demonstrating that the predicted CbbR-binding sites are functional in vitro. However, CbbR failed to bind the upstream region of the cbb4 operon that contains cbbP, encoding phosphoribulokinase (EC 2.7.1.19). Thus, other factors not present in the assay may be required for binding or the region lacks a functional CbbR-binding site. The cbb3 operon contains genes predicted to encode anthranilate synthase components I and II, catalyzing the formation of anthranilate and pyruvate from chorismate. This suggests a novel regulatory connection between CO2 fixation and tryptophan biosynthesis. The presence of a form II RubisCO could promote the ability of A. ferrooxidans to fix CO2 at different concentrations of CO2.ConclusionsA. ferrooxidans has features of cbb gene organization for CO2-assimilating functions that are characteristic of obligate chemolithoautotrophs and distinguish this group from facultative autotrophs. The most conspicuous difference is a separate operon for the cbbP gene. It is hypothesized that this organization may provide greater flexibility in the regulation of expression of genes involved in inorganic carbon assimilation.

Project description:Chemoautotrophy has been little studied in typical coastal marine sediments, but may be an important component of carbon recycling as intense anaerobic mineralization processes in these sediments lead to accumulation of high amounts of reduced compounds, such as sulfides and ammonium. We studied chemoautotrophy by measuring dark-fixation of 13C-bicarbonate into phospholipid derived fatty acid (PLFA) biomarkers at two coastal sediment sites with contrasting sulfur chemistry in the Eastern Scheldt estuary, The Netherlands. At one site where free sulfide accumulated in the pore water right to the top of the sediment, PLFA labeling was restricted to compounds typically found in sulfur and ammonium oxidizing bacteria. At the other site, with no detectable free sulfide in the pore water, a very different PLFA labeling pattern was found with high amounts of label in branched i- and a-PLFA besides the typical compounds for sulfur and ammonium oxidizing bacteria. This suggests that other types of chemoautotrophic bacteria were also active, most likely Deltaproteobacteria related to sulfate reducers. Maximum rates of chemoautotrophy were detected in first 1 to 2 centimeters of both sediments and chemosynthetic biomass production was high ranging from 3 to 36 mmol C m(-2) d(-1). Average dark carbon fixation to sediment oxygen uptake ratios were 0.22±0.07 mol C (mol O2)(-1), which is in the range of the maximum growth yields reported for sulfur oxidizing bacteria indicating highly efficient growth. Chemoautotrophic biomass production was similar to carbon mineralization rates in the top of the free sulfide site, suggesting that chemoautotrophic bacteria could play a crucial role in the microbial food web and labeling in eukaryotic poly-unsaturated PLFA was indeed detectable. Our study shows that dark carbon fixation by chemoautotrophic bacteria is a major process in the carbon cycle of coastal sediments, and should therefore receive more attention in future studies on sediment biogeochemistry and microbial ecology.

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Carbon fixation pathways across the bacterial and archaeal tree of life.

Publications

Carbon fixation pathways across the bacterial and archaeal tree of life.

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