Vitamin B12 Synthesis and Salvage Pathways Were Acquired by Horizontal Gene Transfer to the Thermotogales

Swithers, Kristen S.; Petrus, Amanda K.; Secinaro, Michael A.; Nesbø, Camilla; Gogarten, J. Peter; Noll, Kenneth M.; Butzin, Nicholas C.

doi:10.1093/gbe/evs057

“…africanus were grown on B 12 -deficient medium, TL-1, DB-B, and DB-B with 0.5 g/liter vitamin-free casein (MP Biomedicals), respectively (see Table S1 in the supplemental material). TL-1 was modified from previously used DB-B medium (6). TL-1 medium is different from DB-B medium in that it contains 0.75 g/liter vitamin-free casein (MP Biomedicals) and its pH is 7.2.…”

Section: Methodsmentioning

confidence: 99%

“…africanus cultures were grown to mid-log phase in 100-to 200-ml anaerobic cultures. Boiled cell extracts were prepared as described previously (6). Briefly, cells were centrifuged at 3,441 ϫ g for 10 min.…”

Section: Methodsmentioning

confidence: 99%

“…The cobinamide salvage gene cluster has a patchy distribution among Thermotogales species, and ancestral state reconstruction suggested that this pathway was present in the Thermotogales' most recent common ancestor (6). We made several predictions about the origin of the cobinamide salvage pathway and predicted that Thermotogales species are able to utilize different cobinamides.…”

mentioning

confidence: 98%

“…Our recent study provided strong evidence that this order has acquired two different gene clusters, corrinoid synthesis from the firmicutes and cobinamide salvage gene cluster from various archaeal and bacterial organisms. These gene clusters allow for de novo synthesis of vitamin B 12 , also termed cobalamin (6), and the synthesis of B 12 from partial B 12 molecules, called cobinamides. The B 12 cofactor is required by all domains of life, and de novo synthesis requires over 30 enzymes to produce an active form of B 12 (7).…”

mentioning

confidence: 99%

“…We recently explored the evolutionary origins of B 12 -related genes in the Thermotogales and showed that some members of the order, like the Thermosipho africanus strains, can synthesize B 12 de novo, while another species, like Thermotoga maritima, cannot (6). The cobinamide salvage gene cluster has a patchy distribution among Thermotogales species, and ancestral state reconstruction suggested that this pathway was present in the Thermotogales' most recent common ancestor (6).…”

mentioning

confidence: 99%

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Thermotoga lettingae Can Salvage Cobinamide To Synthesize Vitamin B₁₂

Butzin

¹

,

Secinaro

²

,

Swithers

³

et al. 2013

Appl Environ Microbiol

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We recently reported that the Thermotogales acquired the ability to synthesize vitamin B 12 by acquisition of genes from two distantly related lineages, Archaea and Firmicutes (K. S. Swithers et al., Genome Biol. Evol. 4:730 -739, 2012). Ancestral state reconstruction suggested that the cobinamide salvage gene cluster was present in the Thermotogales' most recent common ancestor. We also predicted that Thermotoga lettingae could not synthesize B 12 de novo but could use the cobinamide salvage pathway to synthesize B 12 . In this study, these hypotheses were tested, and we found that Tt. lettingae did not synthesize B 12 de novo but salvaged cobinamide. The growth rate of Tt. lettingae increased with the addition of B 12 or cobinamide to its medium. It synthesized B 12 when the medium was supplemented with cobinamide, and no B 12 was detected in cells grown on cobinamide-deficient medium. Upstream of the cobinamide salvage genes is a putative B 12 riboswitch. In other organisms, B 12 riboswitches allow for higher transcriptional activity in the absence of B 12 . When Tt. lettingae was grown with no B 12 , the salvage genes were upregulated compared to cells grown with B 12 or cobinamide. Another gene cluster with a putative B 12 riboswitch upstream is the btuFCD ABC transporter, and it showed a transcription pattern similar to that of the cobinamide salvage genes. The BtuF proteins from species that can and cannot salvage cobinamides were shown in vitro to bind both B 12 and cobinamide. These results suggest that Thermotogales species can use the BtuFCD transporter to import both B 12 and cobinamide, even if they cannot salvage cobinamide. The Thermotogales order is one of the deepest bacterial lineages in the "ribosomal tree of life" (1-3). Thermotogales genomes are subjected to frequent gene transfers (4), with the largest number of transfers from archaea and firmicutes (5). Our recent study provided strong evidence that this order has acquired two different gene clusters, corrinoid synthesis from the firmicutes and cobinamide salvage gene cluster from various archaeal and bacterial organisms. These gene clusters allow for de novo synthesis of vitamin B 12 , also termed cobalamin (6), and the synthesis of B 12 from partial B 12 molecules, called cobinamides. The B 12 cofactor is required by all domains of life, and de novo synthesis requires over 30 enzymes to produce an active form of B 12 (7). B 12 is required as a growth factor for many bacteria and archaea that do not have genes for its de novo synthesis. Only 50% of sequenced bacterial genomes that indicate a need for B 12 appear to encode the ability to synthesize B 12 (8). Some of these bacteria salvage incomplete corrinoid rings called cobinamides and use these as precursors to synthesize an active form of B 12 (9). Other microorganisms import B 12 from the environment using a B 12 /cobinamide BtuFCD ABC transporter (10).We recently explored the evolutionary origins of B 12 -related genes in the Thermotogales and showed that some members of the order, l...

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Thermosipho

Nesbø

¹

,

Farrell

²

,

Zhaxybayeva

³

et al. 2022

Bergey's Manual of Systematics of Archaea and Bacteria

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Ther.mo.si'pho. Gr. fem. n. thermê , heat; L. masc. n. sipho , little pipe to suck drinks through, a tube; N.L. masc. n. Thermosipho , the hot tube, due to the sheath surrounding the bacteria. Thermotogota / Thermotogae / Thermotogales / Fervidobacteriaceae / Thermosipho The genus Thermosipho is currently composed of eight species ( Thermosipho africanus , Thermosipho melanesiensis , Thermosipho japonicus , Thermosipho geolei , Thermosipho atlanticus , Thermosipho affectus , Thermosipho globiformans , and Thermosipho activus ). The rods are surrounded by an outer sheath‐like toga, and some rods form spheroids during growth. The spheroids may produce “immature progenies” that are too small to contain a complete genome, which need further investigation to elucidate their function. The cells are obligately anaerobic , thermophilic , with optimum growth temperature of 65–75°C, optimal pH 6.0–7.5, and optimal growth under low salinity 2.0–3.0% NaCl. Heterotrophic growth . Sulfur is reduced to H 2 S by all the species, while thiosulfate is reduced by Thermosipho africanus and Thermosipho japonicus . Molecular hydrogen inhibits growth. Two described Thermosipho spp. are capable of de novo biosynthesis of vitamin B12. Members of the phylum Thermotogota , class Thermotogae , order Thermotogales , and family Fervidobacteriaceae . Known habitats are shallow and deep‐sea hydrothermal vents and deep subsurface oil reservoirs. DNA G + C content (mol%) : 29.5–31.5 ( T m and genome analysis). Type species : Thermosipho africanus Huber et al. 1989, VL31 emend. Ravot et al. 1996.

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Pseudothermotoga

Farrell

¹

,

Nesbø

²

,

Zhaxybayeva

³

et al. 2021

Bergey's Manual of Systematics of Archaea and Bacteria

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0

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Pseu.do.ther.mo.to'ga. Gr. adj. pseudo , false; N.L. fem. n. Thermotoga, a bacterial genus; N.L. fem. n. Pseudothermotoga, a genus falsely (or incorrectly) classified as Thermotoga . Thermotogota / Thermotogae / Thermotogales / Thermotogaceae / Pseudothermotoga The genus Pseudothermotoga comprises sheathed, thermophilic, anaerobic, fermentative, and hydrogen‐producing bacteria. Thiosulfate is reduced by all the strains of the genus. Pseudothermotoga spp. are members of the phylum Thermotogota , class Thermotogae, order Thermotogales , family Thermotogaceae . Known habitats are hot springs, oil reservoirs, and thermophilic bioreactors. Genome sizes are in the range 2.01–2.19 Mb, and GC content varies between 38.7 and 51.3%. Based on phylogenomic analyses, two recently described species, Thermotoga profunda and Thermotoga caldifontis, should be assigned to the recently described genus Pseudothermotoga . Based on DNA–DNA hybridization and various genomic measurements, the Pseudothermotoga lettingae and Pseudothermotoga subterranea species should be reclassified as subspecies of Pseudothermotoga elfii . With these proposed reclassifications, the genus Pseudothermotoga would consist of five described species: Pseudothermotoga thermarum, Pseudothermotoga elfii, Pseudothermotoga hypogea, Pseudothermotoga Profunda, and Pseudothermotoga caldifontis . However, high genomic divergence observed within this genus may require additional taxonomic revisions in the future. DNA G + C content (mol%) : 38.7–51.3. Type species : Pseudothermotoga thermarum Bhandari and Gupta, 2014, VL158 (Basonym: Thermotoga thermarum, Windberger et al. 1989 ).

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Vitamin B12 Synthesis and Salvage Pathways Were Acquired by Horizontal Gene Transfer to the Thermotogales

Cited by 20 publications

References 49 publications

Thermotoga lettingae Can Salvage Cobinamide To Synthesize Vitamin B₁₂

Thermotoga lettingae Can Salvage Cobinamide To Synthesize Vitamin B₁₂

Thermosipho

Pseudothermotoga

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Vitamin B12 Synthesis and Salvage Pathways Were Acquired by Horizontal Gene Transfer to the Thermotogales

Cited by 20 publications

References 49 publications

Thermotoga lettingae Can Salvage Cobinamide To Synthesize Vitamin B12

Thermotoga lettingae Can Salvage Cobinamide To Synthesize Vitamin B12

Thermosipho

Pseudothermotoga

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Product

Resources

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Thermotoga lettingae Can Salvage Cobinamide To Synthesize Vitamin B₁₂

Thermotoga lettingae Can Salvage Cobinamide To Synthesize Vitamin B₁₂