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Title: Unexpected host dependency of Antarctic Nanohaloarchaeota

Abstract

In hypersaline environments, Nanohaloarchaeota (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaeota [DPANN] superphylum) are thought to be free-living microorganisms. We report cultivation of 2 strains of Antarctic Nanohaloarchaeota and show that they require the haloarchaeon Halorubrum lacusprofundi for growth. By performing growth using enrichments and fluorescence-activated cell sorting, we demonstrated successful cultivation of Candidatus Nanohaloarchaeum antarcticus, purification of Ca. Nha. antarcticus away from other species, and growth and verification of Ca. Nha. antarcticus with Hrr. lacusprofundi ; these findings are analogous to those required for fulfilling Koch’s postulates. We use fluorescent in situ hybridization and transmission electron microscopy to assess cell structures and interactions; metagenomics to characterize enrichment taxa, generate metagenome assembled genomes, and interrogate Antarctic communities; and proteomics to assess metabolic pathways and speculate about the roles of certain proteins. Metagenome analysis indicates the presence of a single species, which is endemic to Antarctic hypersaline systems that support the growth of haloarchaea. The presence of unusually large proteins predicted to function in attachment and invasion of hosts plus the absence of key biosynthetic pathways (e.g., lipids) in metagenome assembled genomes of globally distributed Nanohaloarchaeota indicate that all members of the lineage have evolved as symbionts. Our work expands the range ofmore » archaeal symbiotic lifestyles and provides a genetically tractable model system for advancing understanding of the factors controlling microbial symbiotic relationships.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1564400
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 29; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Hamm, Joshua N., Erdmann, Susanne, Eloe-Fadrosh, Emiley A., Angeloni, Allegra, Zhong, Ling, Brownlee, Christopher, Williams, Timothy J., Barton, Kirston, Carswell, Shaun, Smith, Martin A., Brazendale, Sarah, Hancock, Alyce M., Allen, Michelle A., Raftery, Mark J., and Cavicchioli, Ricardo. Unexpected host dependency of Antarctic Nanohaloarchaeota. United States: N. p., 2019. Web. doi:10.1073/pnas.1905179116.
Hamm, Joshua N., Erdmann, Susanne, Eloe-Fadrosh, Emiley A., Angeloni, Allegra, Zhong, Ling, Brownlee, Christopher, Williams, Timothy J., Barton, Kirston, Carswell, Shaun, Smith, Martin A., Brazendale, Sarah, Hancock, Alyce M., Allen, Michelle A., Raftery, Mark J., & Cavicchioli, Ricardo. Unexpected host dependency of Antarctic Nanohaloarchaeota. United States. doi:10.1073/pnas.1905179116.
Hamm, Joshua N., Erdmann, Susanne, Eloe-Fadrosh, Emiley A., Angeloni, Allegra, Zhong, Ling, Brownlee, Christopher, Williams, Timothy J., Barton, Kirston, Carswell, Shaun, Smith, Martin A., Brazendale, Sarah, Hancock, Alyce M., Allen, Michelle A., Raftery, Mark J., and Cavicchioli, Ricardo. Fri . "Unexpected host dependency of Antarctic Nanohaloarchaeota". United States. doi:10.1073/pnas.1905179116.
@article{osti_1564400,
title = {Unexpected host dependency of Antarctic Nanohaloarchaeota},
author = {Hamm, Joshua N. and Erdmann, Susanne and Eloe-Fadrosh, Emiley A. and Angeloni, Allegra and Zhong, Ling and Brownlee, Christopher and Williams, Timothy J. and Barton, Kirston and Carswell, Shaun and Smith, Martin A. and Brazendale, Sarah and Hancock, Alyce M. and Allen, Michelle A. and Raftery, Mark J. and Cavicchioli, Ricardo},
abstractNote = {In hypersaline environments, Nanohaloarchaeota (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaeota [DPANN] superphylum) are thought to be free-living microorganisms. We report cultivation of 2 strains of Antarctic Nanohaloarchaeota and show that they require the haloarchaeon Halorubrum lacusprofundi for growth. By performing growth using enrichments and fluorescence-activated cell sorting, we demonstrated successful cultivation of Candidatus Nanohaloarchaeum antarcticus, purification of Ca. Nha. antarcticus away from other species, and growth and verification of Ca. Nha. antarcticus with Hrr. lacusprofundi ; these findings are analogous to those required for fulfilling Koch’s postulates. We use fluorescent in situ hybridization and transmission electron microscopy to assess cell structures and interactions; metagenomics to characterize enrichment taxa, generate metagenome assembled genomes, and interrogate Antarctic communities; and proteomics to assess metabolic pathways and speculate about the roles of certain proteins. Metagenome analysis indicates the presence of a single species, which is endemic to Antarctic hypersaline systems that support the growth of haloarchaea. The presence of unusually large proteins predicted to function in attachment and invasion of hosts plus the absence of key biosynthetic pathways (e.g., lipids) in metagenome assembled genomes of globally distributed Nanohaloarchaeota indicate that all members of the lineage have evolved as symbionts. Our work expands the range of archaeal symbiotic lifestyles and provides a genetically tractable model system for advancing understanding of the factors controlling microbial symbiotic relationships.},
doi = {10.1073/pnas.1905179116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 29,
volume = 116,
place = {United States},
year = {2019},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1073/pnas.1905179116

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