Reconstructing genomes of carbon monoxide oxidisers in volcanic deposits including members of the class Ktedonobacteria

Abstract

Microorganisms can potentially colonize volcanic rocks using the chemical energy in reduced gases such as methane, hydrogen (H2) and carbon monoxide (CO). In this study, we analysed soil metagenomes from Chilean volcanic soils, representing three different successional stages with ages of 380, 269 and 63 years, respectively. A total of 19 metagenome-assembled genomes (MAGs) were retrieved from all stages with a higher number observed in the youngest soil (1640: 2 MAGs, 1751: 1 MAG, 1957: 16 MAGs). Genomic similarity indices showed that several MAGs had amino-acid identity (AAI) values >50% to the phyla Actinobacteria, Acidobacteria, Gemmatimonadetes, Proteobacteria and Chloroflexi. Three MAGs from the youngest site (1957) belonged to the class Ktedonobacteria (Chloroflexi). Complete cellular functions of all the MAGs were characterised, including carbon fixation, terpenoid backbone biosynthesis, formate oxidation and CO oxidation. All 19 environmental genomes contained at least one gene encoding a putative carbon monoxide dehydrogenase (CODH). Three MAGs had form I coxL operon (encoding the large subunit CO-dehydrogenase). One of these MAGs (MAG-1957-2.1, Ktedonobacterales) was highly abundant in the youngest soil. MAG-1957-2.1 also contained genes encoding a [NiFe]-hydrogenase and hyp genes encoding accessory enzymes and proteins. Little is known about the Ktedonobacterales through cultivated isolates, but some species can utilize H2 and CO for growth. Our results strongly suggest that the remote volcanic sites in Chile represent a natural habitat for Ktedonobacteria and they may use reduced gases for growth.

Reticulibacter mediterranei gen. nov., sp. nov., within the new family Reticulibacteraceae fam. nov., and Ktedonospora formicarum gen. nov., sp. nov., Ktedonobacter robiniae sp. nov., Dictyobacter formicarum sp. nov. and Dictyobacter arantiisoli sp. nov., belonging to the class Ktedonobacteria

“…Therefore, the ability to scavenge trace gas may be a common feature among several members of Ktedonobacteria. Additionally, numerous BGCs (13)(14)(15)(16)(17)(18)(19) for secondary metabolites mainly coding for non-ribosomal peptides, polyketides and ribosomally synthesized and post-translationally modified peptide products were predicted in the genomes of the seven strains (Tables 1 and S3), suggesting that, similarly to other ktedonobacterial strains [12], these strains have a high potential for producing secondary metabolites.…”

“…hazakensis SK20-1 T [13,14]. Interestingly, some members of this class are expected to play an important role in energy cycling in volcanic and oligotrophic terrestrial environments as oxidizers of atmospheric CO and H 2 [15][16][17] Isolates and environmental DNA belonging to this class were found to be ubiquitous in various terrestrial environments and particularly abundant in several organic-poor soils of volcanic environments such as bare Antarctic soils [18], volcanic soils [19] and geothermally heated soils [20]. Several isolates (SOSP and Uno series), some of which may represent novel taxa in the class, have been isolated by our groups but have not been formally described [1,4].…”

“…hazakensis SK20-1 T [13, 14]. Interestingly, some members of this class are expected to play an important role in energy cycling in volcanic and oligotrophic terrestrial environments as oxidizers of atmospheric CO and H 2 [15–17]…”

Tree phyllospheres are a habitat for diverse populations of CO-oxidising bacteria

“…Carboxydotrophs and carboxydovores are taxonomically diverse, including members of the Proteobacteria, Firmicutes, Actinobacteria, Chloroflexi and Bacteroidetes identified in marine [47][48][49], soil [48,50,51] and rhizosphere environments [45,48]. The presence of coxL genes in a wide range of environments and in representatives of uncultivated clades of bacteria indicates that the diversity of CO-oxidising bacteria is greater than those currently identified by cultivation [49,[52][53][54][55][56][57][58]. CO oxidation is known to enhance the long-term survival of some bacteria, supporting their persistence in deprived or changeable environments [59] and recent research indicates that CO oxidation may be a more generalist function than previously assumed, with 56% of soil bacteria predicted to be capable of CO oxidation [60].…”