Detection of anaerobic carbon monoxide-oxidizing thermophiles in hydrothermal environments

Yoneda, Yasuko; Kano, Sanae; Yoshida, Takashi; Ikeda, Eitaro; Fukuyama, Yuto; Omae, Kimiho; Kimura-Sakai, Shigeko; Daifuku, Takashi; Watanabe, Tetsuyou; Sako, Yoshihiko

doi:10.1093/femsec/fiv093

Cited by 16 publications

(20 citation statements)

References 37 publications

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“…Anaerobic CO-oxidizing bacteria have been detected in geothermal springs of neutral pH (Brady et al, 2015). In addition, anaerobic microbial CO consumption has been observed in acidic hot spring mud of pH 2.9 (Ikeda et al, 2015). In both cases, the microbial population was dominated by Firmicutes.…”

Section: Introductionmentioning

confidence: 97%

Hydrogen and Carbon Monoxide-Utilizing Kyrpidia spormannii Species From Pantelleria Island, Italy

et al. 2020

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Volcanic and geothermal areas are hot and often acidic environments that emit geothermal gasses, including H 2 , CO and CO 2. Geothermal gasses mix with air, creating conditions where thermoacidophilic aerobic H 2-and CO-oxidizing microorganisms could thrive. Here, we describe the isolation of two Kyrpidia spormannii strains, which can grow autotrophically by oxidizing H 2 and CO with oxygen. These strains, FAVT5 and COOX1, were isolated from the geothermal soils of the Favara Grande on Pantelleria Island, Italy. Extended physiology studies were performed with K. spormannii FAVT5, and showed that this strain grows optimally at 55 • C and pH 5.0. The highest growth rate is obtained using H 2 as energy source (µ max 0.19 ± 0.02 h −1 , doubling time 3.6 h). K. spormannii FAVT5 can additionally grow on a variety of organic substrates, including some alcohols, volatile fatty acids and amino acids. The genome of each strain encodes for two O 2-tolerant hydrogenases belonging to [NiFe] group 2a hydrogenases and transcriptome studies using K. spormannii FAVT5 showed that both hydrogenases are expressed under H 2 limiting conditions. So far no Firmicutes except K. spormannii FAVT5 have been reported to exhibit a high affinity for H 2 , with a K s of 327 ± 24 nM. The genomes of each strain encode for one putative CO dehydrogenase, belonging to Form II aerobic CO dehydrogenases. The genomic potential and physiological properties of these Kyrpidia strains seem to be quite well adapted to thrive in the harsh environmental volcanic conditions.

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Section: Introductionmentioning

confidence: 97%

Hydrogen and Carbon Monoxide-Utilizing Kyrpidia spormannii Species From Pantelleria Island, Italy

et al. 2020

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“…Although a number of strains of Moorella thermoacetica have been isolated, only one strain ( M. thermoacetica strain AMP) exhibits hydrogenogenic carboxydotrophy, whereas the other strains are acetogenic carboxydotrophs (Jiang et al 2009 ). Because of their ability to use potentially toxic CO and produce H 2 as the source of energy for other microbes, hydrogenogenic carboxydotrophs are assumed to be important ‘CO scavengers’ and primary producers in the environment (Sokolova and Lebedinsky 2013 ; Techtmann et al 2009 ; Yoneda et al 2013 , 2015 ).…”

Section: Introductionmentioning

confidence: 99%

Transcriptome analysis of a thermophilic and hydrogenogenic carboxydotroph Carboxydothermus pertinax

et al. 2019

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A thermophilic and hydrogenogenic carboxydotroph, Carboxydothermus pertinax, performs hydrogenogenic CO metabolism in which CODH-II couples with distally encoded ECH. To enhance our knowledge of its hydrogenogenic CO metabolism, we performed whole transcriptome analysis of C. pertinax grown under 100% CO or 100% N 2 using RNA sequencing. Of the 2577 genes, 36 and 64 genes were differentially expressed genes (DEGs) with false discovery rate adjusted P value < 0.05 when grown under 100% CO or 100% N 2 , respectively. Most of the DEGs were components of 23 gene clusters, suggesting switch between metabolisms via intensive expression changes in a relatively low number of gene clusters. Of the 9 significantly expressed gene clusters under 100% CO, CODH-II and ECH gene clusters were found. Only the ECH gene cluster was regulated by the CO-responsive transcriptional factor CooA, suggesting that others were separately regulated in the same transcriptional cascade as the ECH gene cluster. Of the 14 significantly expressed gene clusters under 100% N 2 , ferrous iron transport gene cluster involved in anaerobic respiration and prophage region were found. Considering that the expression of the temperate phage was strictly repressed under 100% CO, hydrogenogenic CO metabolism might be stable for C. pertinax . Electronic supplementary material The online version of this article (10.1007/s00792-019-01091-x) contains supplementary material, which is available to authorized users.

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“…A number of prokaryotes are capable of using CO as an electron donor, and some of them can also use CO as a carbon source ( King and Weber, 2007 ; Oelgeschläger and Rother, 2008 ; Sokolova and Lebedinsky, 2013 ; Tiquia-Arashiro, 2014 ; Diender et al, 2015 ). In various terrestrial hydrotherms, potential activity or the presence of CO-oxidizing anaerobes has been revealed ( Kochetkova et al, 2011 ; Brady et al, 2015 ; Yoneda et al, 2015 ), and the number of newly isolated CO-oxidizers is increasing permanently ( Balk et al, 2009 ; Yoneda et al, 2012 , 2013 ; Sokolova and Lebedinsky, 2013 ; Tiquia-Arashiro, 2014 ). Among cultivated thermophilic anaerobic CO-oxidizing species, hydrogenogenic carboxydotrophs are in majority, moreover, in certain hot springs, they comprise a significant portion of the microbial population ( Yoneda et al, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

“…In various terrestrial hydrotherms, potential activity or the presence of CO-oxidizing anaerobes has been revealed ( Kochetkova et al, 2011 ; Brady et al, 2015 ; Yoneda et al, 2015 ), and the number of newly isolated CO-oxidizers is increasing permanently ( Balk et al, 2009 ; Yoneda et al, 2012 , 2013 ; Sokolova and Lebedinsky, 2013 ; Tiquia-Arashiro, 2014 ). Among cultivated thermophilic anaerobic CO-oxidizing species, hydrogenogenic carboxydotrophs are in majority, moreover, in certain hot springs, they comprise a significant portion of the microbial population ( Yoneda et al, 2015 ). These bacteria oxidize carbon monoxide via the following reaction: CO + H 2 O → CO 2 + H 2 (ΔG 0′ = -20 kJ).…”

Section: Introductionmentioning

confidence: 99%

Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals

et al. 2018

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The genus Carboxydocella forms a deeply branching family in the class Clostridia and is currently represented by three physiologically diverse species of thermophilic prokaryotes. The type strain of the type species, Carboxydocella thermautotrophica 41T, is an obligate chemolithoautotroph growing exclusively by hydrogenogenic CO oxidation. Another strain, isolated from a hot spring at Uzon caldera, Kamchatka in the course of this work, is capable of coupling carboxydotrophy and dissimilatory reduction of Fe(III) from oxic and phyllosilicate minerals. The processes of carboxydotrophy and Fe(III) reduction appeared to be interdependent in this strain. The genomes of both isolates were sequenced, assembled into single chromosome sequences (for strain 41T a plasmid sequence was also assembled) and analyzed. Genome analysis revealed that each of the two strains possessed six genes encoding diverse Ni,Fe-containing CO dehydrogenases (maximum reported in complete prokaryotic genomes), indicating crucial role of carbon monoxide in C. thermautotrophica metabolism. Both strains possessed a set of 30 multiheme c-type cytochromes, but only the newly isolated Fe-reducing strain 019 had one extra gene of a 17-heme cytochrome, which is proposed to represent a novel determinant of dissimilatory iron reduction in prokaryotes. Mössbauer studies revealed that strain 019 induced reductive transformation of the abundant ferric/ferrous-mica mineral glauconite to siderite during carboxydotrophic growth. Reconstruction of the C. thermautotrophica strains energy metabolism is the first comprehensive genome analysis of a representative of the deep phylogenetic branch Clostridia Incertae Sedis, family V. Our data provide insights into energy metabolism of C. thermautotrophica with an emphasis on its ecological implications.

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Detection of anaerobic carbon monoxide-oxidizing thermophiles in hydrothermal environments

Cited by 16 publications

References 37 publications

Hydrogen and Carbon Monoxide-Utilizing Kyrpidia spormannii Species From Pantelleria Island, Italy

Hydrogen and Carbon Monoxide-Utilizing Kyrpidia spormannii Species From Pantelleria Island, Italy

Transcriptome analysis of a thermophilic and hydrogenogenic carboxydotroph Carboxydothermus pertinax

Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals

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