TY - JOUR
T1 - Respiratory pathways Reconstructed by multi-omics analysis in Melioribacter roseus, residing in a deep thermal aquifer of the west-siberian megabasin
AU - Gavrilov, Sergey
AU - Podosokorskaya, Olga
AU - Alexeev, Dmitry
AU - Merkel, Alexander
AU - Khomyakova, Maria
AU - Muntyan, Maria
AU - Altukhov, Ilya
AU - Butenko, Ivan
AU - Bonch-Osmolovskaya, Elizaveta
AU - Govorun, Vadim
AU - Kublanov, Ilya
N1 - Publisher Copyright:
© 2017 Gavrilov, Podosokorskaya, Alexeev, Merkel, Khomyakova, Muntyan, Altukhov, Butenko, Bonch-Osmolovskaya, Govorun and Kublanov.
PY - 2017/6/30
Y1 - 2017/6/30
N2 - Melioribacter roseus, a representative of recently proposed Ignavibacteriae phylum, is a metabolically versatile thermophilic bacterium, inhabiting subsurface biosphere of the West-Siberian megabasin and capable of growing on various substrates and electron acceptors. Genomic analysis followed by inhibitor studies and membrane potential measurements of aerobically grown M. roseus cells revealed the activity of aerobic respiratory electron transfer chain comprised of respiratory complexes I and IV, and an alternative complex III. Phylogeny reconstruction revealed that oxygen reductases belonged to atypical cc(o/b)o3-type and canonical cbb3-type cytochrome oxidases. Also, two molybdoenzymes of M. roseus were affiliated either with Ttr or Psr/Phs clades, but not with typical respiratory arsenate reductases of the Arr clade. Expression profiling, both at transcripts and protein level, allowed us to assign the role of the terminal respiratory oxidase under atmospheric oxygen concentration for the cc(o/b)o3 cytochrome oxidase, previously proposed to serve for oxygen detoxification only. Transcriptomic analysis revealed the involvement of both molybdoenzymes of M. roseus in As(V) respiration, yet differences in the genomic context of their gene clusters allow to hypothesize about their distinct roles in arsenate metabolism with the 'Psr/Phs'-type molybdoenzyme being the most probable candidate respiratory arsenate reductase. Basing on multi-omics data, the pathways for aerobic and arsenate respiration were proposed. Our results start to bridge the vigorously increasing gap between homology-based predictions and experimentally verified metabolic processes, what is especially important for understudied microorganisms of novel lineages from deep subsurface environments of Eurasia, which remained separated from the rest of the biosphere for several geological periods.
AB - Melioribacter roseus, a representative of recently proposed Ignavibacteriae phylum, is a metabolically versatile thermophilic bacterium, inhabiting subsurface biosphere of the West-Siberian megabasin and capable of growing on various substrates and electron acceptors. Genomic analysis followed by inhibitor studies and membrane potential measurements of aerobically grown M. roseus cells revealed the activity of aerobic respiratory electron transfer chain comprised of respiratory complexes I and IV, and an alternative complex III. Phylogeny reconstruction revealed that oxygen reductases belonged to atypical cc(o/b)o3-type and canonical cbb3-type cytochrome oxidases. Also, two molybdoenzymes of M. roseus were affiliated either with Ttr or Psr/Phs clades, but not with typical respiratory arsenate reductases of the Arr clade. Expression profiling, both at transcripts and protein level, allowed us to assign the role of the terminal respiratory oxidase under atmospheric oxygen concentration for the cc(o/b)o3 cytochrome oxidase, previously proposed to serve for oxygen detoxification only. Transcriptomic analysis revealed the involvement of both molybdoenzymes of M. roseus in As(V) respiration, yet differences in the genomic context of their gene clusters allow to hypothesize about their distinct roles in arsenate metabolism with the 'Psr/Phs'-type molybdoenzyme being the most probable candidate respiratory arsenate reductase. Basing on multi-omics data, the pathways for aerobic and arsenate respiration were proposed. Our results start to bridge the vigorously increasing gap between homology-based predictions and experimentally verified metabolic processes, what is especially important for understudied microorganisms of novel lineages from deep subsurface environments of Eurasia, which remained separated from the rest of the biosphere for several geological periods.
KW - Arsenate reductase
KW - Cytochrome oxidases
KW - Deep subsurface environment
KW - Respiratory metabolism
KW - Thermophilic bacteria
KW - West-Siberian megabasin
UR - http://www.scopus.com/inward/record.url?scp=85021910097&partnerID=8YFLogxK
U2 - 10.3389/fmicb.2017.01228
DO - 10.3389/fmicb.2017.01228
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AN - SCOPUS:85021910097
SN - 1664-302X
VL - 8
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
IS - JUN
M1 - 1228
ER -