Phylogeny and Metabolic Potential of the Methanotrophic Lineage MO3 in Beijerinckiaceae from the Paddy Soil through Metagenome-Assembled Genome Reconstruction

Although the study of aerobic methane-oxidizing bacteria (MOB, methanotrophs) has been carried out for more than a hundred years, there are many uncultivated methanotrophic lineages whose metabolism is largely unknown. Here, we reconstructed a nearly complete genome of a Beijerinckiaceae methanotrop...

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Main Authors: Yuanfeng Cai, Juanli Yun, Zhongjun Jia
Format: Article
Language:English
Published: MDPI AG 2022-05-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/10/5/955
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author Yuanfeng Cai
Juanli Yun
Zhongjun Jia
author_facet Yuanfeng Cai
Juanli Yun
Zhongjun Jia
author_sort Yuanfeng Cai
collection DOAJ
description Although the study of aerobic methane-oxidizing bacteria (MOB, methanotrophs) has been carried out for more than a hundred years, there are many uncultivated methanotrophic lineages whose metabolism is largely unknown. Here, we reconstructed a nearly complete genome of a Beijerinckiaceae methanotroph from the enrichment of paddy soil by using nitrogen-free M2 medium. The methanotroph labeled as MO3_YZ.1 had a size of 3.83 Mb, GC content of 65.6%, and 3442 gene-coding regions. Based on phylogeny of <i>pmoA</i> gene and genome and the genomic average nucleotide identity, we confirmed its affiliation to the MO3 lineage and a close relationship to <i>Methylocapsa</i>. MO3_YZ.1 contained <i>mxaF</i>- and <i>xoxF</i>-type methanol dehydrogenase. MO3_YZ.1 used the serine cycle to assimilate carbon and regenerated glyoxylate through the glyoxylate shunt as it contained isocitrate lyase and complete tricarboxylic acid cycle-coding genes. The ethylmalonyl-CoA pathway and Calvin–Benson–Bassham cycle were incomplete in MO3_YZ.1. Three acetate utilization enzyme-coding genes were identified, suggesting its potential ability to utilize acetate. The presence of genes for N<sub>2</sub> fixation, sulfur transformation, and poly-β-hydroxybutyrate synthesis enable its survival in heterogeneous habitats with fluctuating supplies of carbon, nitrogen, and sulfur.
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spelling doaj.art-eaa9783560e9469f984232038719d1662023-11-23T12:15:34ZengMDPI AGMicroorganisms2076-26072022-05-0110595510.3390/microorganisms10050955Phylogeny and Metabolic Potential of the Methanotrophic Lineage MO3 in Beijerinckiaceae from the Paddy Soil through Metagenome-Assembled Genome ReconstructionYuanfeng Cai0Juanli Yun1Zhongjun Jia2State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, ChinaAlthough the study of aerobic methane-oxidizing bacteria (MOB, methanotrophs) has been carried out for more than a hundred years, there are many uncultivated methanotrophic lineages whose metabolism is largely unknown. Here, we reconstructed a nearly complete genome of a Beijerinckiaceae methanotroph from the enrichment of paddy soil by using nitrogen-free M2 medium. The methanotroph labeled as MO3_YZ.1 had a size of 3.83 Mb, GC content of 65.6%, and 3442 gene-coding regions. Based on phylogeny of <i>pmoA</i> gene and genome and the genomic average nucleotide identity, we confirmed its affiliation to the MO3 lineage and a close relationship to <i>Methylocapsa</i>. MO3_YZ.1 contained <i>mxaF</i>- and <i>xoxF</i>-type methanol dehydrogenase. MO3_YZ.1 used the serine cycle to assimilate carbon and regenerated glyoxylate through the glyoxylate shunt as it contained isocitrate lyase and complete tricarboxylic acid cycle-coding genes. The ethylmalonyl-CoA pathway and Calvin–Benson–Bassham cycle were incomplete in MO3_YZ.1. Three acetate utilization enzyme-coding genes were identified, suggesting its potential ability to utilize acetate. The presence of genes for N<sub>2</sub> fixation, sulfur transformation, and poly-β-hydroxybutyrate synthesis enable its survival in heterogeneous habitats with fluctuating supplies of carbon, nitrogen, and sulfur.https://www.mdpi.com/2076-2607/10/5/955methanotrophglyoxylate shuntpaddy soilmetagenome-assembled genome<i>pmoA</i>
spellingShingle Yuanfeng Cai
Juanli Yun
Zhongjun Jia
Phylogeny and Metabolic Potential of the Methanotrophic Lineage MO3 in Beijerinckiaceae from the Paddy Soil through Metagenome-Assembled Genome Reconstruction
Microorganisms
methanotroph
glyoxylate shunt
paddy soil
metagenome-assembled genome
<i>pmoA</i>
title Phylogeny and Metabolic Potential of the Methanotrophic Lineage MO3 in Beijerinckiaceae from the Paddy Soil through Metagenome-Assembled Genome Reconstruction
title_full Phylogeny and Metabolic Potential of the Methanotrophic Lineage MO3 in Beijerinckiaceae from the Paddy Soil through Metagenome-Assembled Genome Reconstruction
title_fullStr Phylogeny and Metabolic Potential of the Methanotrophic Lineage MO3 in Beijerinckiaceae from the Paddy Soil through Metagenome-Assembled Genome Reconstruction
title_full_unstemmed Phylogeny and Metabolic Potential of the Methanotrophic Lineage MO3 in Beijerinckiaceae from the Paddy Soil through Metagenome-Assembled Genome Reconstruction
title_short Phylogeny and Metabolic Potential of the Methanotrophic Lineage MO3 in Beijerinckiaceae from the Paddy Soil through Metagenome-Assembled Genome Reconstruction
title_sort phylogeny and metabolic potential of the methanotrophic lineage mo3 in beijerinckiaceae from the paddy soil through metagenome assembled genome reconstruction
topic methanotroph
glyoxylate shunt
paddy soil
metagenome-assembled genome
<i>pmoA</i>
url https://www.mdpi.com/2076-2607/10/5/955
work_keys_str_mv AT yuanfengcai phylogenyandmetabolicpotentialofthemethanotrophiclineagemo3inbeijerinckiaceaefromthepaddysoilthroughmetagenomeassembledgenomereconstruction
AT juanliyun phylogenyandmetabolicpotentialofthemethanotrophiclineagemo3inbeijerinckiaceaefromthepaddysoilthroughmetagenomeassembledgenomereconstruction
AT zhongjunjia phylogenyandmetabolicpotentialofthemethanotrophiclineagemo3inbeijerinckiaceaefromthepaddysoilthroughmetagenomeassembledgenomereconstruction