The Chthonomonas calidirosea Genome Is Highly Conserved across Geographic Locations and Distinct Chemical and Microbial Environments in New Zealand's Taupō Volcanic Zone

Abstract

Chthonomonas calidirosea T49T is a low-abundance, carbohydrate-scavenging, and thermophilic soil bacterium with a seemingly disorganized genome. We hypothesized that the C. calidirosea genome would be highly responsive to local selection pressure, resulting in the divergence of its genomic content, genome organization, and carbohydrate utilization phenotype across environments. We tested this hypothesis by sequencing the genomes of four C. calidirosea isolates obtained from four separate geothermal fields in the Taupō Volcanic Zone, New Zealand. For each isolation site, we measured physicochemical attributes and defined the associated microbial community by 16S rRNA gene sequencing. Despite their ecological and geographical isolation, the genome sequences showed low divergence (maximum, 1.17%). Isolate-specific variations included single-nucleotide polymorphisms (SNPs), restriction-modification systems, and mobile elements but few major deletions and no major rearrangements. The 50-fold variation in C. calidirosea relative abundance among the four sites correlated with site environmental characteristics but not with differences in genomic content. Conversely, the carbohydrate utilization profiles of the C. calidirosea isolates corresponded to the inferred isolate phylogenies, which only partially paralleled the geographical relationships among the sample sites. Genomic sequence conservation does not entirely parallel geographic distance, suggesting that stochastic dispersal and localized extinction, which allow for rapid population homogenization with little restriction by geographical barriers, are possible mechanisms of C. calidirosea distribution. This dispersal and extinction mechanism is likely not limited to C. calidirosea but may shape the populations and genomes of many other low-abundance free-living taxa.IMPORTANCE This study compares the genomic sequence variations and metabolisms of four strains of Chthonomonas calidirosea, a rare thermophilic bacterium from the phylum Armatimonadetes. It additionally compares the microbial communities and chemistry of each of the geographically distinct sites from which the four C. calidirosea strains were isolated. C. calidirosea was previously reported to possess a highly disorganized genome, but it was unclear whether this reflected rapid evolution. Here, we show that each isolation site has a distinct chemistry and microbial community, but despite this, the C. calidirosea genome is highly conserved across all isolation sites. Furthermore, genomic sequence differences only partially paralleled geographic distance, suggesting that C. calidirosea genotypes are not primarily determined by adaptive evolution. Instead, the presence of C. calidirosea may be driven by stochastic dispersal and localized extinction. This ecological mechanism may apply to many other low-abundance taxa.

Mixotrophy drives niche expansion of verrucomicrobial methanotrophs

“…To infer the microorganisms responsible for CH 4 and H 2 uptake, we determined the microbial community structure of the soil profile. Consistent with findings in other acidic soil ecosystems ( Golyshina, 2011 ; Sharp et al , 2014 ; Lee et al , 2016 ), the euryarchaeotal order Thermoplasmatales was dominant at all depths. Methanotrophic verrucomicrobial genera, specifically Methylacidiphilum spp.…”

The Characterization of Microbiome and Interactions on Weathered Rocks in a Subsurface Karst Cave, Central China

“…For example, Conexibacter stalactiti was isolated from samples of stalactites collected from a lava cave ( Lee, 2017 ), and Actinomadura namibiensis was isolated from desert sandy soil in Namibia ( Wink et al, 2003 ). Chthonomonas calidirosea was thermophilic and isolated from geothermal soil ( Lee K. C. et al, 2016 ; Compton et al, 2020 ). Microbes in the aphotic zone can also be involved in iron reduction.…”

Bacterial communities at a groundwater‐surface water ecotone: gradual change or abrupt transition points along a contamination gradient?

“…The type strain of Chthonomonas , C . calidirosea , has been extracted from geothermally heated soils with low nitrate concentrations (Lee et al ., 2011, 2016). Hyphomicrobium ( Alphaproteobacteria ) strains are chemolithotrophs known to be an important component of groundwater ecosystems (Griebler and Lueders, 2009).…”

“…Several bacterial ESVs, such as the genera Chthonomonas, Hyphomicrobium and the class Saccharimonadales were only found in reference springs; when NO 3 À -N concentration increased even slightly, these taxa vanished rapidly. The type strain of Chthonomonas, C. calidirosea, has been extracted from geothermally heated soils with low nitrate concentrations (Lee et al, 2011(Lee et al, , 2016. Hyphomicrobium (Alphaproteobacteria) strains are chemolithotrophs known to be an important component of groundwater ecosystems (Griebler and Lueders, 2009).…”