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Title: Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis

Nanoarchaeota are obligate symbionts of other Archaea first discovered 16 years ago, yet little is known about this largely uncultivated taxon. While Nanoarchaeota diversity has been detected in a variety of habitats using 16S rRNA gene surveys, genome sequences have been available for only three Nanoarchaeota and their hosts. The host range and adaptation of Nanoarchaeota to a wide range of environmental conditions has thus largely remained elusive. Single-cell genomics is an ideal approach to address these questions as Nanoarchaeota can be isolated while still attached to putative hosts, enabling the exploration of cell-cell interactions and fine-scale genomic diversity. Results: From 22 single amplified genomes (SAGs) from three hot springs in Yellowstone National Park, we derived a genome-based phylogeny of the phylum Nanoarchaeota, linking it to global 16S rRNA gene diversity. By exploiting sequencing of co-sorted tightly attached cells, we associated Nanoarchaeota with 6 novel putative hosts, 2 of which were found in multiple SAGs, and showed that the same host species may associate with multiple species of Nanoarchaeota. Comparison of single nucleotide polymorphisms (SNPs) within a population of Nanoarchaeota SAGs indicated that Nanoarchaeota attached to a single host cell in situ are likely clonal. In addition to an overallmore » pattern of purifying selection, we found significantly higher densities of non-synonymous SNPs in hypothetical cell surface proteins, as compared to other functional categories. Genes implicated in interactions in other obligate microbe-microbe symbioses, including those encoding a cytochrome bd-I ubiquinol oxidase and a FlaJ/TadC homologue possibly involved in type IV pili production, also had relatively high densities of non-synonymous SNPs. Conclusions: This population genetics study of Nanoarchaeota greatly expands the known potential host range of the phylum and hints at what genes may be involved in adaptation to diverse environments or different hosts. We provide the first evidence that Nanoarchaeota cells attached to the same host cell are clonal and propose a hypothesis for how clonality may occur despite diverse symbiont populations.« less
Authors:
ORCiD logo [1] ;  [1] ;  [2] ;  [3] ;  [1] ;  [3] ;  [1] ;  [3] ;  [3] ;  [4] ;  [1] ; ORCiD logo [1] ;  [5] ; ORCiD logo [1]
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  3. Montana State Univ., Bozeman, MT (United States)
  4. Montana State Univ., Bozeman, MT (United States); Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
  5. Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
Publication Date:
Grant/Contract Number:
AC02-05CH11231
Type:
Accepted Manuscript
Journal Name:
Microbiome
Additional Journal Information:
Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
BioMed Central
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Nanoarchaeota; Single-cell genomics; Symbiosis; Single nucleotide polymorphisms
OSTI Identifier:
1477383

Jarett, Jessica K., Nayfach, Stephen, Podar, Mircea, Inskeep, William, Ivanova, Natalia N., Munson-McGee, Jacob, Schulz, Frederik, Young, Mark, Jay, Zackary J., Beam, Jacob P., Kyrpides, Nikos C., Malmstrom, Rex R., Stepanauskas, Ramunas, and Woyke, Tanja. Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis. United States: N. p., Web. doi:10.1186/s40168-018-0539-8.
Jarett, Jessica K., Nayfach, Stephen, Podar, Mircea, Inskeep, William, Ivanova, Natalia N., Munson-McGee, Jacob, Schulz, Frederik, Young, Mark, Jay, Zackary J., Beam, Jacob P., Kyrpides, Nikos C., Malmstrom, Rex R., Stepanauskas, Ramunas, & Woyke, Tanja. Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis. United States. doi:10.1186/s40168-018-0539-8.
Jarett, Jessica K., Nayfach, Stephen, Podar, Mircea, Inskeep, William, Ivanova, Natalia N., Munson-McGee, Jacob, Schulz, Frederik, Young, Mark, Jay, Zackary J., Beam, Jacob P., Kyrpides, Nikos C., Malmstrom, Rex R., Stepanauskas, Ramunas, and Woyke, Tanja. 2018. "Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis". United States. doi:10.1186/s40168-018-0539-8. https://www.osti.gov/servlets/purl/1477383.
@article{osti_1477383,
title = {Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis},
author = {Jarett, Jessica K. and Nayfach, Stephen and Podar, Mircea and Inskeep, William and Ivanova, Natalia N. and Munson-McGee, Jacob and Schulz, Frederik and Young, Mark and Jay, Zackary J. and Beam, Jacob P. and Kyrpides, Nikos C. and Malmstrom, Rex R. and Stepanauskas, Ramunas and Woyke, Tanja},
abstractNote = {Nanoarchaeota are obligate symbionts of other Archaea first discovered 16 years ago, yet little is known about this largely uncultivated taxon. While Nanoarchaeota diversity has been detected in a variety of habitats using 16S rRNA gene surveys, genome sequences have been available for only three Nanoarchaeota and their hosts. The host range and adaptation of Nanoarchaeota to a wide range of environmental conditions has thus largely remained elusive. Single-cell genomics is an ideal approach to address these questions as Nanoarchaeota can be isolated while still attached to putative hosts, enabling the exploration of cell-cell interactions and fine-scale genomic diversity. Results: From 22 single amplified genomes (SAGs) from three hot springs in Yellowstone National Park, we derived a genome-based phylogeny of the phylum Nanoarchaeota, linking it to global 16S rRNA gene diversity. By exploiting sequencing of co-sorted tightly attached cells, we associated Nanoarchaeota with 6 novel putative hosts, 2 of which were found in multiple SAGs, and showed that the same host species may associate with multiple species of Nanoarchaeota. Comparison of single nucleotide polymorphisms (SNPs) within a population of Nanoarchaeota SAGs indicated that Nanoarchaeota attached to a single host cell in situ are likely clonal. In addition to an overall pattern of purifying selection, we found significantly higher densities of non-synonymous SNPs in hypothetical cell surface proteins, as compared to other functional categories. Genes implicated in interactions in other obligate microbe-microbe symbioses, including those encoding a cytochrome bd-I ubiquinol oxidase and a FlaJ/TadC homologue possibly involved in type IV pili production, also had relatively high densities of non-synonymous SNPs. Conclusions: This population genetics study of Nanoarchaeota greatly expands the known potential host range of the phylum and hints at what genes may be involved in adaptation to diverse environments or different hosts. We provide the first evidence that Nanoarchaeota cells attached to the same host cell are clonal and propose a hypothesis for how clonality may occur despite diverse symbiont populations.},
doi = {10.1186/s40168-018-0539-8},
journal = {Microbiome},
number = 1,
volume = 6,
place = {United States},
year = {2018},
month = {9}
}

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