An evaluation of Thiomicrospira, Hydrogenovibrio and Thioalkalimicrobium: reclassification of four species of Thiomicrospira to each Thiomicrorhabdus gen. nov. and Hydrogenovibrio, and reclassification of all four species of Thioalkalimicrobium to Thiomicrospira

Boden, Rich; Scott, Kathleen M.; Williams, John T.; Russel, Sydney; Antonen, Kirsten; Rae, Alex; Hutt, Lee P.

doi:10.1099/ijsem.0.001855

Cited by 120 publications

(74 citation statements)

References 30 publications

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“…to Thiomicrospira spp. (26) is also supported by ANI and AF values ( Fig. S4C), as these species form a cluster that is well separated from the type species of genera in the family Piscirickettsiaceae.…”

supporting

confidence: 61%

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A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

Barco

Scott

Amend

et al. 2020

mBio

247

232

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Genus assignment is fundamental in the characterization of microbes, yet there is currently no unambiguous way to demarcate genera solely using standard genomic relatedness indices. Here, we propose an approach to demarcate genera that relies on the combined use of the average nucleotide identity, genome alignment fraction, and the distinction between type- and non-type species. More than 3,500 genomes representing type strains of species from >850 genera of either bacterial or archaeal lineages were tested. Over 140 genera were analyzed in detail within the taxonomic context of order/family. Significant genomic differences between members of a genus and type species of other genera in the same order/family were conserved in 94% of the cases. Nearly 90% (92% if polyphyletic genera are excluded) of the type strains were classified in agreement with current taxonomy. The 448 type strains that need reclassification directly impact 33% of the genera analyzed in detail. The results provide a first line of evidence that the combination of genomic indices provides added resolution to effectively demarcate genera within the taxonomic framework that is currently based on the 16S rRNA gene. We also identify the emergence of natural breakpoints at the genome level that can further help in the circumscription of taxa, increasing the proportion of directly impacted genera to at least 43% and pointing at inaccuracies on the use of the 16S rRNA gene as a taxonomic marker, despite its precision. Altogether, these results suggest that genomic coherence is an emergent property of genera in Bacteria and Archaea. IMPORTANCE In recent decades, the taxonomy of Bacteria and Archaea, and therefore genus designation, has been largely based on the use of a single ribosomal gene, the 16S rRNA gene, as a taxonomic marker. We propose an approach to delineate genera that excludes the direct use of the 16S rRNA gene and focuses on a standard genome relatedness index, the average nucleotide identity. Our findings are of importance to the microbiology community because the emergent properties of Bacteria and Archaea that are identified in this study will help assign genera with higher taxonomic resolution.

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confidence: 61%

“…S4A). Boden et al (26) recently provided a detailed evaluation of the characteristics of this cluster, which falls within the radiation of the Piscirickettsiaceae and is proposed to place many of the species into different genera. We tested these newly proposed assignments using the approach described above and the MiSI method.…”

mentioning

confidence: 99%

A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

Barco

Scott

Amend

et al. 2020

mBio

247

232

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“…These organisms, namely Acidithiobacillus, Advenella, Halothiobacillus,Pusillimonas and 355 Thiomicrospira, can well increase tetrathionate availability in the ASOMZ sediments, even as they themselves are potential users of the tetrathionate (Kelly and Wood, 2000;Sievert et al, 2000;Boden et al, 2017). Tetrathionate can also be formed in situ, as an intermediate of sulfate/sulfite reduction, by members of the genera Desulfovibrio and Desulfobulbus , which were detected along both the cores via direct taxonomic annotation of the 360 unassembled metagenomic data (see Tables S8 and S9 for the percentages of metagenomic reads ascribed to these genera in the different sediment-samples).…”

Section: Synchronized Population-fluctuation Of Different Tetrathionamentioning

confidence: 99%

“…3). Whilst all members of these genera are known to oxidize tetrathionate to sulfate (Kelly and Wood, 2000;Sievert et al, 2000;Boden et al, 2017), several such genera were also detected (via direct annotation of metagenomic reads) along SSK42/5 and 6, some chemolithotrophic members of which are known to oxidize tetrathionate to sulfate. 370…”

Section: Synchronized Population-fluctuation Of Different Tetrathionamentioning

confidence: 99%

Cryptic role of tetrathionate in the sulfur cycle: A study from Arabian Sea oxygen minimum zone sediments

Mandal

Bhattacharya

Roy

et al. 2019

Preprint

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To explore the potential role of tetrathionate in the sulfur cycle of marine sediments, the population ecology of tetrathionate-forming, oxidizing, and respiring microorganisms was revealed at 15-30 cm resolution along two, ~3-m-long, cores collected from 530-and 580-mbsl water-depths of Arabian Sea, off India's west coast, within the oxygen minimum zone (OMZ). Metagenome analysis along the two 25 sediment-cores revealed widespread occurrence of the structural genes that govern these metabolisms;high diversity and relative-abundance was also detected for the bacteria known to render these processes. Slurry-incubation of the sediment-samples, pure-culture isolation, and metatranscriptome analysis, corroborated the in situ functionality of all the three metabolic-types. Geochemical analyses revealed thiosulfate (0-11.1 µM), pyrite (0.05-1.09 wt %), iron (9232-17234 ppm) and manganese (71-172 30 ppm) along the two sediment-cores. Pyrites (via abiotic reaction with MnO2) and thiosulfate (via oxidation by chemolithotrophic bacteria prevalent in situ) are apparently the main sources of tetrathionate in this ecosystem. Tetrathionate, in turn, can be either converted to sulfate (via oxidation by the chemolithotrophs present) or reduced back to thiosulfate (via respiration by native bacteria); 0-2.01 mM sulfide present in the sediment-cores may also reduce tetrathionate abiotically to thiosulfate and elemental sulfur. Notably 35 tetrathionate was not detected in situ -high microbiological and geochemical reactivity of this polythionate is apparently instrumental in the cryptic nature of its potential role as a central sulfur cycle intermediate.Biogeochemical roles of this polythionate, albeit revealed here in the context of OMZ sediments, may well extend to the sulfur cycles of other geomicrobiologically-distinct marine sediment horizons.

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“…Several members of the genera Thiomicrospira, Thiomicrorhabdus, and Hydrogenovibrio, organisms taxonomically affiliated with H. crunogenus (18), have had their genomes sequenced. Taxa for sequencing were selected to represent both the taxonomic breadth of these genera and the range of habitats from which these organisms have been isolated, including shallow and deep-sea hydrothermal vents, coastal sediments, and soda and salt lakes (19).…”

mentioning

confidence: 99%

Diversity in CO ₂ -Concentrating Mechanisms among Chemolithoautotrophs from the Genera Hydrogenovibrio , Thiomicrorhabdus , and Thiomicrospira , Ubiquitous in Sulfidic Habitats Worldwide

Scott

Leonard

Boden

et al. 2019

Appl Environ Microbiol

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Members of the generaHydrogenovibrio,Thiomicrospira, andThiomicrorhabdusfix carbon at hydrothermal vents, coastal sediments, hypersaline lakes, and other sulfidic habitats. The genome sequences of these ubiquitous and prolific chemolithoautotrophs suggest a surprising diversity of mechanisms for the uptake and fixation of dissolved inorganic carbon (DIC); these mechanisms are verified here. Carboxysomes are apparent in the transmission electron micrographs of most of these organisms but are lacking inThiomicrorhabdussp. strain Milos-T2 andThiomicrorhabdus arctica, and the inability ofThiomicrorhabdussp. strain Milos-T2 to grow under low-DIC conditions is consistent with the absence of carboxysome loci in its genome. For the remaining organisms, genes encoding potential DIC transporters from four evolutionarily distinct families (Tcr_0853 and Tcr_0854, Chr, SbtA, and SulP) are located downstream of carboxysome loci. Transporter genes collocated with carboxysome loci, as well as some homologs located elsewhere on the chromosomes, had elevated transcript levels under low-DIC conditions, as assayed by reverse transcription-quantitative PCR (qRT-PCR). DIC uptake was measureable via silicone oil centrifugation when a representative of each of the four types of transporter was expressed inEscherichia coli. The expression of these genes in the carbonic anhydrase-deficientE. colistrain EDCM636 enabled it to grow under low-DIC conditions, a result consistent with DIC transport by these proteins. The results from this study expand the range of DIC transporters within the SbtA and SulP transporter families, verify DIC uptake by transporters encoded byTcr_0853andTcr_0854and their homologs, and introduce DIC as a potential substrate for transporters from the Chr family.IMPORTANCEAutotrophic organisms take up and fix DIC, introducing carbon into the biological portion of the global carbon cycle. The mechanisms for DIC uptake and fixation by autotrophicBacteriaandArchaeaare likely to be diverse but have been well characterized only for “Cyanobacteria.” Based on genome sequences, members of the generaHydrogenovibrio,Thiomicrospira, andThiomicrorhabdushave a variety of mechanisms for DIC uptake and fixation. We verified that most of these organisms are capable of growing under low-DIC conditions, when they upregulate carboxysome loci and transporter genes collocated with these loci on their chromosomes. When these genes, which fall into four evolutionarily independent families of transporters, are expressed inE. coli, DIC transport is detected. This expansion in known DIC transporters across four families, from organisms from a variety of environments, provides insight into the ecophysiology of autotrophs, as well as a toolkit for engineering microorganisms for carbon-neutral biochemistries of industrial importance.

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An evaluation of Thiomicrospira, Hydrogenovibrio and Thioalkalimicrobium: reclassification of four species of Thiomicrospira to each Thiomicrorhabdus gen. nov. and Hydrogenovibrio, and reclassification of all four species of Thioalkalimicrobium to Thiomicrospira

Cited by 120 publications

References 30 publications

A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

Cryptic role of tetrathionate in the sulfur cycle: A study from Arabian Sea oxygen minimum zone sediments

Diversity in CO ₂ -Concentrating Mechanisms among Chemolithoautotrophs from the Genera Hydrogenovibrio , Thiomicrorhabdus , and Thiomicrospira , Ubiquitous in Sulfidic Habitats Worldwide

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An evaluation of Thiomicrospira, Hydrogenovibrio and Thioalkalimicrobium: reclassification of four species of Thiomicrospira to each Thiomicrorhabdus gen. nov. and Hydrogenovibrio, and reclassification of all four species of Thioalkalimicrobium to Thiomicrospira

Cited by 120 publications

References 30 publications

A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

Cryptic role of tetrathionate in the sulfur cycle: A study from Arabian Sea oxygen minimum zone sediments

Diversity in CO 2 -Concentrating Mechanisms among Chemolithoautotrophs from the Genera Hydrogenovibrio , Thiomicrorhabdus , and Thiomicrospira , Ubiquitous in Sulfidic Habitats Worldwide

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Diversity in CO ₂ -Concentrating Mechanisms among Chemolithoautotrophs from the Genera Hydrogenovibrio , Thiomicrorhabdus , and Thiomicrospira , Ubiquitous in Sulfidic Habitats Worldwide