Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”

“Candidatus Nitrosocaldaceae” are globally distributed in neutral or slightly alkaline hot springs and geothermally heated soils. Despite their essential role in the nitrogen cycle in high-temperature ecosystems, they remain poorly understood because they have never been isolated in pure culture, an...

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Main Authors: Zhen-Hao Luo, Manik Prabhu Narsing Rao, Hao Chen, Zheng-Shuang Hua, Qi Li, Brian P. Hedlund, Zhou-Yan Dong, Bing-Bing Liu, Shu-Xian Guo, Wen-Sheng Shu, Wen-Jun Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.608832/full
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author Zhen-Hao Luo
Manik Prabhu Narsing Rao
Hao Chen
Zheng-Shuang Hua
Zheng-Shuang Hua
Qi Li
Brian P. Hedlund
Brian P. Hedlund
Zhou-Yan Dong
Bing-Bing Liu
Shu-Xian Guo
Wen-Sheng Shu
Wen-Jun Li
Wen-Jun Li
spellingShingle Zhen-Hao Luo
Manik Prabhu Narsing Rao
Hao Chen
Zheng-Shuang Hua
Zheng-Shuang Hua
Qi Li
Brian P. Hedlund
Brian P. Hedlund
Zhou-Yan Dong
Bing-Bing Liu
Shu-Xian Guo
Wen-Sheng Shu
Wen-Jun Li
Wen-Jun Li
Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”
Frontiers in Microbiology
“Candidatus Nitrosocaldaceae”
hot spring
ammonia-oxidizing archaea
genome comparison
horizontal gene transfer
author_facet Zhen-Hao Luo
Manik Prabhu Narsing Rao
Hao Chen
Zheng-Shuang Hua
Zheng-Shuang Hua
Qi Li
Brian P. Hedlund
Brian P. Hedlund
Zhou-Yan Dong
Bing-Bing Liu
Shu-Xian Guo
Wen-Sheng Shu
Wen-Jun Li
Wen-Jun Li
author_sort Zhen-Hao Luo
title Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”
title_short Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”
title_full Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”
title_fullStr Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”
title_full_unstemmed Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”
title_sort genomic insights of “candidatus nitrosocaldaceae” based on nine new metagenome-assembled genomes, including “candidatus nitrosothermus” gen nov. and two new species of “candidatus nitrosocaldus”
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-01-01
description “Candidatus Nitrosocaldaceae” are globally distributed in neutral or slightly alkaline hot springs and geothermally heated soils. Despite their essential role in the nitrogen cycle in high-temperature ecosystems, they remain poorly understood because they have never been isolated in pure culture, and very few genomes are available. In the present study, a metagenomics approach was employed to obtain “Ca. Nitrosocaldaceae” metagenomic-assembled genomes (MAGs) from hot spring samples collected from India and China. Phylogenomic analysis placed these MAGs within “Ca. Nitrosocaldaceae.” Average nucleotide identity and average amino acid identity analysis suggested the new MAGs represent two novel species of “Candidatus Nitrosocaldus” and a novel genus, herein proposed as “Candidatus Nitrosothermus.” Key genes responsible for chemolithotrophic ammonia oxidation and a thaumarchaeal 3HP/4HB cycle were detected in all MAGs. Furthermore, genes coding for urea degradation were only present in “Ca. Nitrosocaldus,” while biosynthesis of the vitamins, biotin, cobalamin, and riboflavin were detected in almost all MAGs. Comparison of “Ca. Nitrosocaldales/Nitrosocaldaceae” with other AOA revealed 526 specific orthogroups. This included genes related to thermal adaptation (cyclic 2,3-diphosphoglycerate, and S-adenosylmethionine decarboxylase), indicating their importance for life at high temperature. In addition, these MAGs acquired genes from members from archaea (Crenarchaeota) and bacteria (Firmicutes), mainly involved in metabolism and stress responses, which might play a role to allow this group to adapt to thermal habitats.
topic “Candidatus Nitrosocaldaceae”
hot spring
ammonia-oxidizing archaea
genome comparison
horizontal gene transfer
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.608832/full
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spelling doaj-44dec13f18d241349ed42b621cf800e22021-01-08T04:36:11ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-01-011110.3389/fmicb.2020.608832608832Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”Zhen-Hao Luo0Manik Prabhu Narsing Rao1Hao Chen2Zheng-Shuang Hua3Zheng-Shuang Hua4Qi Li5Brian P. Hedlund6Brian P. Hedlund7Zhou-Yan Dong8Bing-Bing Liu9Shu-Xian Guo10Wen-Sheng Shu11Wen-Jun Li12Wen-Jun Li13State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaDepartment of Biological Sciences, Dartmouth College, Hanover, NH, United StatesState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, University of Nevada, Las Vegas, Las Vegas, NV, United StatesNevada Institute of Personalized Medicine, University of Nevada, Las Vegas, Las Vegas, NV, United StatesState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaHenan Key Laboratory of Industrial Microbial Resources and Fermentation Technology, College of Biological and Chemical Engineering, Nanyang Institute of Technology, Nanyang, ChinaHenan Key Laboratory of Industrial Microbial Resources and Fermentation Technology, College of Biological and Chemical Engineering, Nanyang Institute of Technology, Nanyang, ChinaSchool of Life Sciences, South China Normal University, Guangzhou, ChinaState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaHenan Key Laboratory of Industrial Microbial Resources and Fermentation Technology, College of Biological and Chemical Engineering, Nanyang Institute of Technology, Nanyang, China“Candidatus Nitrosocaldaceae” are globally distributed in neutral or slightly alkaline hot springs and geothermally heated soils. Despite their essential role in the nitrogen cycle in high-temperature ecosystems, they remain poorly understood because they have never been isolated in pure culture, and very few genomes are available. In the present study, a metagenomics approach was employed to obtain “Ca. Nitrosocaldaceae” metagenomic-assembled genomes (MAGs) from hot spring samples collected from India and China. Phylogenomic analysis placed these MAGs within “Ca. Nitrosocaldaceae.” Average nucleotide identity and average amino acid identity analysis suggested the new MAGs represent two novel species of “Candidatus Nitrosocaldus” and a novel genus, herein proposed as “Candidatus Nitrosothermus.” Key genes responsible for chemolithotrophic ammonia oxidation and a thaumarchaeal 3HP/4HB cycle were detected in all MAGs. Furthermore, genes coding for urea degradation were only present in “Ca. Nitrosocaldus,” while biosynthesis of the vitamins, biotin, cobalamin, and riboflavin were detected in almost all MAGs. Comparison of “Ca. Nitrosocaldales/Nitrosocaldaceae” with other AOA revealed 526 specific orthogroups. This included genes related to thermal adaptation (cyclic 2,3-diphosphoglycerate, and S-adenosylmethionine decarboxylase), indicating their importance for life at high temperature. In addition, these MAGs acquired genes from members from archaea (Crenarchaeota) and bacteria (Firmicutes), mainly involved in metabolism and stress responses, which might play a role to allow this group to adapt to thermal habitats.https://www.frontiersin.org/articles/10.3389/fmicb.2020.608832/full“Candidatus Nitrosocaldaceae”hot springammonia-oxidizing archaeagenome comparisonhorizontal gene transfer