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Title: Metabolic versatility of small archaea Micrarchaeota and Parvarchaeota

Abstract

Small acidophilic archaea belonging to Micrarchaeota and Parvarchaeota phyla are known to physically interact with some Thermoplasmatales members in nature. However, due to a lack of cultivation and limited genomes on hand, their biodiversity, metabolisms, and physiologies remain largely unresolved. For this study, we obtained 39 genomes from acid mine drainage (AMD) and hot spring environments around the world. 16S rRNA gene based analyses revealed that Parvarchaeota were only detected in AMD and hot spring habitats, while Micrarchaeota were also detected in others including soil, peat, hypersaline mat, and freshwater, suggesting a considerable higher diversity and broader than expected habitat distribution for this phylum. Despite their small genomes (0.64-1.08 Mb), these archaea may contribute to carbon and nitrogen cycling by degrading multiple saccharides and proteins, and produce ATP via aerobic respiration and fermentation. Additionally, we identified several syntenic genes with homology to those involved in iron oxidation in six Parvarchae ota genomes, suggesting their potential role in iron cycling. However, both phyla lack biosynthetic pathways for amino acids and nucleotides, suggesting that they likely scavenge these biomolecules from the environment and/or other community members. Moreover, low-oxygen enrichments in laboratory confirmed our speculation that both phyla are microaerobic/anaerobic, based on severalmore » specific genes identified in them. Furthermore, phylogenetic analyses provide insights into the close evolutionary history of energy related functionalities between both phyla with Thermoplasmatales. These results expand our understanding of these elusive archaea by revealing their involvement in carbon, nitrogen, and iron cycling, and suggest their potential interactions with Thermoplasmatales on genomic scale.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [5];  [1];  [1];  [1];  [6];  [1];  [7];  [5];  [1];  [8];  [8];  [9];  [3];  [10]
  1. Sun Yat-Sen Univ., Guangzhou, (China). State Key Lab. of Biocontrol, Guangdong Key Lab. of Plant Resources and College of Ecology and Evolution
  2. Univ. of Oviedo (Spain). Dept. of Functional Biology and Univ. Inst. of Biotechnology of Asturias (IUBA); Univ. of Illinois, Urbana, IL (United States). Carl R. Woese Inst. for Genomic Biology
  3. Univ. of Texas, Austin, TX (United States). Dept. of Marine Science and Marine Science Inst.
  4. National Autonomous Univ. of Mexico, Morelia (Mexico). Lab. of Microbiomics and National School of Higher Studies Morelia
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Yunnan Univ., Kunming (China). Yunnan Inst. of Microbiology
  7. National Autonomous Univ. of Mexico, Morelia (Mexico). Dept. of Ecological Genomics and Center for Genomic Sciences
  8. Univ. of Oviedo (Spain). Dept. of Functional Biology and Univ. Inst. of Biotechnology of Asturias (IUBA)
  9. Spanish National Research Council (CSIC), Madrid (Spain). Inst. of Catalysis
  10. South China Normal Univ., Guangzhou (China). School of Life Sciences
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Univ. of California, Berkeley, CA (United States); National Center for Biotechnology Information (NCBI); China Univ. of Geosciences, Wuhan (China); Univ. of Massachusetts, Amherst, MA (United States); Univ. of Konstanz (Germany); National Natural Science Foundation of China (NNSFC); Alfred P. Sloan Foundation; National Autonomous Univ. of Mexico, Morelia (Mexico)
OSTI Identifier:
1434028
Grant/Contract Number:  
AC02-05CH11231; 31600101; U1201233; 31570500; PAPIIT IA210617
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 12; Journal Issue: 3; Related Information: © 2017 The Author(s) 2017, under exclusive licence to Macmillan Publishers Limited, part of Springer Nature.; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Metagenomics; Water microbiology

Citation Formats

Chen, Lin-Xing, Mendez-Garcia, Celia, Dombrowski, Nina, Servin-Garciduenas, Luis E., Eloe-Fadrosh, Emiley A., Fang, Bao-Zhu, Luo, Zhen-Hao, Tan, Sha, Zhi, Xiao-Yang, Hua, Zheng-Shuang, Martinez-Romero, Esperanza, Woyke, Tanja, Huang, Li-Nan, Sanchez, Jesus, Pelaez, Ana Isabel, Ferrer, Manuel, Baker, Brett J., and Shu, Wen-Sheng. Metabolic versatility of small archaea Micrarchaeota and Parvarchaeota. United States: N. p., 2017. Web. doi:10.1038/s41396-017-0002-z.
Chen, Lin-Xing, Mendez-Garcia, Celia, Dombrowski, Nina, Servin-Garciduenas, Luis E., Eloe-Fadrosh, Emiley A., Fang, Bao-Zhu, Luo, Zhen-Hao, Tan, Sha, Zhi, Xiao-Yang, Hua, Zheng-Shuang, Martinez-Romero, Esperanza, Woyke, Tanja, Huang, Li-Nan, Sanchez, Jesus, Pelaez, Ana Isabel, Ferrer, Manuel, Baker, Brett J., & Shu, Wen-Sheng. Metabolic versatility of small archaea Micrarchaeota and Parvarchaeota. United States. doi:10.1038/s41396-017-0002-z.
Chen, Lin-Xing, Mendez-Garcia, Celia, Dombrowski, Nina, Servin-Garciduenas, Luis E., Eloe-Fadrosh, Emiley A., Fang, Bao-Zhu, Luo, Zhen-Hao, Tan, Sha, Zhi, Xiao-Yang, Hua, Zheng-Shuang, Martinez-Romero, Esperanza, Woyke, Tanja, Huang, Li-Nan, Sanchez, Jesus, Pelaez, Ana Isabel, Ferrer, Manuel, Baker, Brett J., and Shu, Wen-Sheng. Fri . "Metabolic versatility of small archaea Micrarchaeota and Parvarchaeota". United States. doi:10.1038/s41396-017-0002-z. https://www.osti.gov/servlets/purl/1434028.
@article{osti_1434028,
title = {Metabolic versatility of small archaea Micrarchaeota and Parvarchaeota},
author = {Chen, Lin-Xing and Mendez-Garcia, Celia and Dombrowski, Nina and Servin-Garciduenas, Luis E. and Eloe-Fadrosh, Emiley A. and Fang, Bao-Zhu and Luo, Zhen-Hao and Tan, Sha and Zhi, Xiao-Yang and Hua, Zheng-Shuang and Martinez-Romero, Esperanza and Woyke, Tanja and Huang, Li-Nan and Sanchez, Jesus and Pelaez, Ana Isabel and Ferrer, Manuel and Baker, Brett J. and Shu, Wen-Sheng},
abstractNote = {Small acidophilic archaea belonging to Micrarchaeota and Parvarchaeota phyla are known to physically interact with some Thermoplasmatales members in nature. However, due to a lack of cultivation and limited genomes on hand, their biodiversity, metabolisms, and physiologies remain largely unresolved. For this study, we obtained 39 genomes from acid mine drainage (AMD) and hot spring environments around the world. 16S rRNA gene based analyses revealed that Parvarchaeota were only detected in AMD and hot spring habitats, while Micrarchaeota were also detected in others including soil, peat, hypersaline mat, and freshwater, suggesting a considerable higher diversity and broader than expected habitat distribution for this phylum. Despite their small genomes (0.64-1.08 Mb), these archaea may contribute to carbon and nitrogen cycling by degrading multiple saccharides and proteins, and produce ATP via aerobic respiration and fermentation. Additionally, we identified several syntenic genes with homology to those involved in iron oxidation in six Parvarchae ota genomes, suggesting their potential role in iron cycling. However, both phyla lack biosynthetic pathways for amino acids and nucleotides, suggesting that they likely scavenge these biomolecules from the environment and/or other community members. Moreover, low-oxygen enrichments in laboratory confirmed our speculation that both phyla are microaerobic/anaerobic, based on several specific genes identified in them. Furthermore, phylogenetic analyses provide insights into the close evolutionary history of energy related functionalities between both phyla with Thermoplasmatales. These results expand our understanding of these elusive archaea by revealing their involvement in carbon, nitrogen, and iron cycling, and suggest their potential interactions with Thermoplasmatales on genomic scale.},
doi = {10.1038/s41396-017-0002-z},
journal = {The ISME Journal},
number = 3,
volume = 12,
place = {United States},
year = {2017},
month = {12}
}

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    Works referencing / citing this record:

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