Newly Identified Nematodes from Mono Lake Exhibit Extreme Arsenic Resistance
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.
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.Attached Files
Supplemental Material - 1-s2.0-S0960982219310401-mmc1.pdf
Supplemental Material - 1-s2.0-S0960982219310401-mmc2.pdf
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Additional details
- Eprint ID
- 98870
- DOI
- 10.1016/j.cub.2019.08.024
- Resolver ID
- CaltechAUTHORS:20190926-092428868
- Amgen
- Leverhulme Trust
- RPG-2016-089
- Howard Hughes Medical Institute (HHMI)
- Created
-
2019-09-26Created from EPrint's datestamp field
- Updated
-
2021-11-16Created from EPrint's last_modified field