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Colonial choanoflagellate isolated from Mono Lake harbors a microbiome

K. H. Hake, P.T. West, K. McDonald, D. Laundon, A. Garcia De Las Bayonas, C. Feng, View ORCID ProfileP. Burkhardt, D.J. Richter, J.F. Banfield, View ORCID ProfileN. King
doi: https://doi.org/10.1101/2021.03.30.437421
K. H. Hake
1Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA
2Calico Life Sciences, South San Francisco, CA, USA
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P.T. West
3Department of Environmental Science, Policy, & Management, University of California, Berkeley, CA, USA
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K. McDonald
4Electron Microscopy Laboratory, University of California, Berkeley, CA, USA
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D. Laundon
5Marine Biological Association of the United Kingdom, Plymouth, United Kingdom
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A. Garcia De Las Bayonas
1Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA
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C. Feng
1Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA
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P. Burkhardt
5Marine Biological Association of the United Kingdom, Plymouth, United Kingdom
6Sars International Centre for Molecular Marine Biology, University of Bergen, Bergen, Norway
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  • ORCID record for P. Burkhardt
D.J. Richter
7Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain
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J.F. Banfield
3Department of Environmental Science, Policy, & Management, University of California, Berkeley, CA, USA
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N. King
1Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA
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  • ORCID record for N. King
  • For correspondence: nking@berkeley.edu
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ABSTRACT

Choanoflagellates offer key insights into bacterial influences on the origin and early evolution of animals. Here we report the isolation and characterization of a new colonial choanoflagellate species, Barroeca monosierra, that, unlike previously characterized species, harbors a microbiome. B. monosierra was isolated from Mono Lake, California and forms large spherical colonies that are more than an order of magnitude larger than those formed by the closely related Salpingoeca rosetta. By designing fluorescence in situ hybridization probes from metagenomic sequences, we found that B. monosierra colonies are colonized by members of the halotolerant and closely related Saccharospirillaceae and Oceanospirillaceae, as well as purple sulfur bacteria (Ectothiorhodospiraceae) and non-sulfur Rhodobacteraceae. This relatively simple microbiome in a close relative of animals presents a new experimental model for investigating the evolution of stable interactions among eukaryotes and bacteria.

IMPORTANCE The animals and bacteria of Mono Lake (California) have evolved diverse strategies for surviving the hypersaline, alkaline, arsenic-rich environment. We sought to investigate whether the closest living relatives of animals, the choanoflagellates, exist among the relatively limited diversity of organisms in Mono Lake. We repeatedly isolated members of a single species of choanoflagellate, which we have named Barroeca monosierra, suggesting that it is a stable and abundant part of the ecosystem. Characterization of B. monosierra revealed that it forms large spherical colonies that each contain a microbiome, providing an opportunity to investigate the evolution of stable physical associations between eukaryotes and bacteria.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • 1. Added analysis of bacterial community overlap across samples (Fig. S15) 2. Added table summarizing metagenomic sequencing outcomes (Table S2) 3. Added table of dereplicated bin sets used for ribosomal protein tree (Table S8) 4. Revised methods section 5. Minor copy-editing

  • https://www.protocols.io/view/16s-rrna-probe-design-for-hcr-fish-wdffa3n

  • https://www.protocols.io/edit/hcr-fish-for-choanoflagellate-cultures-wddfa26/steps

  • https://doi.org/10.6084/m9.figshare.14474214

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted November 10, 2021.
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Colonial choanoflagellate isolated from Mono Lake harbors a microbiome
K. H. Hake, P.T. West, K. McDonald, D. Laundon, A. Garcia De Las Bayonas, C. Feng, P. Burkhardt, D.J. Richter, J.F. Banfield, N. King
bioRxiv 2021.03.30.437421; doi: https://doi.org/10.1101/2021.03.30.437421
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Colonial choanoflagellate isolated from Mono Lake harbors a microbiome
K. H. Hake, P.T. West, K. McDonald, D. Laundon, A. Garcia De Las Bayonas, C. Feng, P. Burkhardt, D.J. Richter, J.F. Banfield, N. King
bioRxiv 2021.03.30.437421; doi: https://doi.org/10.1101/2021.03.30.437421

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