Genomic analysis of the mesophilic Thermotogae genus Mesotoga reveals phylogeographic structure and genomic determinants of its distinct metabolism

Abstract

Summary The genus Mesotoga, the only described mesophilic Thermotogae lineage, is common in mesothermic anaerobic hydrocarbon‐rich environments. Besides mesophily, Mesotoga displays lineage‐specific phenotypes, such as no or little H2 production and dependence on sulfur‐compound reduction, which may influence its ecological role. We used comparative genomics of 18 Mesotoga strains (pairwise 16S rRNA identity >99%) and a transcriptome of M. prima to investigate how life at moderate temperatures affects phylogeography and to interrogate the genomic features of its lineage‐specific metabolism. We propose that Mesotoga accomplish H2 oxidation and thiosulfate reduction using a sulfide dehydrogenase and a hydrogenase‐complex and that a pyruvate:ferredoxin oxidoreductase acquired from Clostridia is responsible for oxidizing acetate. Phylogenetic analysis revealed three distinct Mesotoga lineages (89.6%–99.9% average nucleotide identity [ANI] within lineages, 79.3%–87.6% ANI between lineages) having different geographic distribution patterns and high levels of intra‐lineage recombination but little geneflow between lineages. Including data from metagenomes, phylogeographic patterns suggest that geographical separation historically has been more important for Mesotoga than hyperthermophilic Thermotoga and we hypothesize that distribution of Mesotoga is constrained by their anaerobic lifestyle. Our data also suggest that recent anthropogenic activities and environments (e.g., wastewater treatment, oil exploration) have expanded Mesotoga habitats and dispersal capabilities.

Comparison of different cultures and culturing conditions for the biological deterioration of organic load from real saline bilge wastewater: microbial diversity insights and ecotoxicity assessment

“…Nitrosococcus genus are Ammonia Oxidizing Bacteria (AOB), adapted to saline and acidic environments, regularly found in marine environments but less commonly detected in waste water treatment reactors (Fumasoli et al 2017). Mesotoga are frequently found in oil-polluted marine mesophilic anaerobic environments (Nesbø et al 2019). Brooklawnia species are nonmotile, mesophilic, neutrophilic facultative anaerobic bacteria that have been previously identified in chlorosolvent-contaminated environments (da Costa et al 2015) and Syntrophorhabdus are as well nonmotile, mesophilic but strictly anaerobic bacteria, metabolizing simple aromatic compounds (Kuever 2014).…”

Newly identified proviruses in Thermotogota suggest that viruses are the vehicles on the highways of interphylum gene sharing

“…The phylum Thermotogota comprises anaerobic fermentative bacteria, most of which are thermophiles (Pollo et al ., 2015). They are common in subsurface environments such as marine vents, terrestrial hot springs and deep subsurface oil reservoirs (Bhandari and Gupta, 2014; Nesbø et al ., 2015, 2019; Foght et al ., 2017). On phylogenetic trees of 16S rRNA gene, Thermotogota is usually a deep branching bacterial lineage, while ribosomal proteins and other markers do not always agree with that placement (Zhaxybayeva et al ., 2009; Hug et al ., 2016).…”

“…Moreover, although both prokaryotic cell and virus numbers decrease with depth, the virus-to-cell ratio can increase with depth (Anderson et al, 2013;Engelhardt et al, 2014;Walsh et al, 2016). Phylogeographic studies of hyperthermophilic Thermotoga and mesophilic Mesotoga have revealed genetic interaction between geographically distant populations, particularly among the hyperthermophilic Thermotoga (Nesbø et al, 2015(Nesbø et al, , 2019). Viruses are one potential source of such long-distance dispersal of genetic material (Ochman et al, 2000), especially for anaerobic organisms where surface dispersal is problematic.…”

Newly identified proviruses in Thermotogota suggest that viruses are the vehicles on the highways of interphylum gene sharing

“…The phylum Thermotogota comprises anaerobic fermentative bacteria, most of which are thermophiles [1]. They are found as a deep branching lineage in some universal phylogenetic trees, for example those made from 16S rRNA genes [2], and are common in subsurface environments such as marine vents, terrestrial hot springs and deep subsurface oil reservoirs [3] [4][5][6].…”

“…Homologous recombination among closely related genomes is another important evolutionary force acting on Thermotogota genomes [4, 9]. For both the Thermotoga and Mesotoga genera, comparative genomic analyses and analyses of homologous recombination have shown that long fragments of DNA (> 10,000 nucleotides) are transferred between closely related strains [6]. Both types of gene-sharing processes might be driven by viruses.…”