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Newly Identified Nematodes from Mono Lake Exhibit Extreme Arsenic Resistance

Shih, Pei-Yin and Lee, James Siho and Shinya, Ryoji and Kanzaki, Natsumi and Pires-daSilva, Andre and Badroos, Jean Marie and Goetz, Elizabeth and Sapir, Amir and Sternberg, Paul W. (2019) Newly Identified Nematodes from Mono Lake Exhibit Extreme Arsenic Resistance. Current Biology, 29 (19). pp. 3339-3344. ISSN 0960-9822. https://resolver.caltech.edu/CaltechAUTHORS:20190926-092428868

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Abstract

Extremophiles have much to reveal about the biology of resilience, yet their study is limited by sampling and culturing difficulties [1, 2, 3]. The broad success and small size of nematodes make them advantageous for tackling these problems [4, 5, 6]. We investigated the arsenic-rich, alkaline, and hypersaline Mono Lake (CA, US) [7, 8, 9] for extremophile nematodes. Though Mono Lake has previously been described to contain only two animal species (brine shrimp and alkali flies) in its water and sediments [10], we report the discovery of eight nematode species from the lake, including microbe grazers, parasites, and predators. Thus, nematodes are the dominant animals of Mono Lake in species richness. Phylogenetic analysis suggests that the nematodes originated from multiple colonization events, which is striking, given the young history of extreme conditions at Mono Lake [7, 11]. One species, Auanema sp., is new, culturable, and survives 500 times the human lethal dose of arsenic. Comparisons to two non-extremophile sister species [12] reveal that arsenic resistance is a common feature of the genus and a preadaptive trait that likely allowed Auanema to inhabit Mono Lake. This preadaptation may be partly explained by a variant in the gene dbt-1 shared with some Caenorhabditis elegans natural populations and known to confer arsenic resistance [13]. Our findings expand Mono Lake’s ecosystem from two known animal species to ten, and they provide a new system for studying arsenic resistance. The dominance of nematodes in Mono Lake and other extreme environments and our findings of preadaptation to arsenic raise the intriguing possibility that nematodes are widely pre-adapted to be extremophiles.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.cub.2019.08.024DOIArticle
ORCID:
AuthorORCID
Shih, Pei-Yin0000-0003-3082-9242
Kanzaki, Natsumi0000-0001-8752-1674
Sapir, Amir0000-0001-9888-1800
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2019 Elsevier Ltd. Received 7 March 2019, Revised 24 May 2019, Accepted 9 August 2019, Available online 26 September 2019. We thank Dr. Avi BarMassada for the map of Mono Lake, Dr. Stephanie A. Connon for advice on collecting and preserving samples from Mono Lake, Dr. Tim Hollibaugh for suggestions on replicating Mono Lake conditions in the laboratory, Prof. Joe Parker for suggestions on building phylogenetic trees, Prof. Tsui-Fen Chou for advice on calculating relative arsenic resistance, and Dr. Nathan Dalleska at the Environmental Analysis Center at Caltech for help on soil property measurements. J.M.B. was supported by the Amgen Scholars Program. A.P.-d.S. acknowledges funding by Leverhulme Trust (RPG-2016-089). P.W.S was an investigator with the Howard Hughes Medical Institute, which supported this work. Author Contributions: Conceptualization, P.-Y.S., J.S.L., R.S., A.S., and P.W.S.; Formal Analysis, P.-Y.S., J.S.L., R.S., N.K., A.P.-d.S., and A.S; Investigation, P.-Y.S., J.S.L., R.S., N.K., A.P.-d.S., J.M.B., and A.S.; Resources, A.P.-d.S., E.G., and A.S.; Writing – Original Draft, P.-Y.S., and J.S.L.; Writing – Review & Editing, P.-Y.S., J.S.L., R.S., N.K., E.G., A.S., and P.W.S.; Visualization, P.-Y.S., J.S.L., R.S., and N.K.; Supervision, A.S. and P.W.S.; Funding Acquisition, P.W.S. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
AmgenUNSPECIFIED
Leverhulme TrustRPG-2016-089
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:Mono Lake; arsenic; extremophiles; nematodes; preadaptation; resilience
Issue or Number:19
Record Number:CaltechAUTHORS:20190926-092428868
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190926-092428868
Official Citation:Pei-Yin Shih, James Siho Lee, Ryoji Shinya, Natsumi Kanzaki, Andre Pires-daSilva, Jean Marie Badroos, Elizabeth Goetz, Amir Sapir, Paul W. Sternberg, Newly Identified Nematodes from Mono Lake Exhibit Extreme Arsenic Resistance, Current Biology, Volume 29, Issue 19, 2019, Pages 3339-3344.e4, ISSN 0960-9822, https://doi.org/10.1016/j.cub.2019.08.024. (http://www.sciencedirect.com/science/article/pii/S0960982219310401)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:98870
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:26 Sep 2019 16:39
Last Modified:11 Oct 2019 18:02

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