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Synergistic epistasis enhances cooperativity of mutualistic interspecies interactions

Turkarslan, Serdar and Stopnisek, Nejc and Thompson, Anne W. and Arens, Christina E. and Valenzuela, Jacob J. and Wilson, James and Hunt, Kristopher A. and Hardwicke, Jessica and Lim, Sujung and Seah, Yee Mey and Fu, Ying and Wu, Liyou and Zhou, Jizhong and Hillesland, Kristina L. and Stahl, David A. and Baliga, Nitin S. (2020) Synergistic epistasis enhances cooperativity of mutualistic interspecies interactions. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20200626-103612993

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Abstract

Frequent fluctuations in sulfate availability rendered syntrophic interactions between the sulfate reducing bacterium Desulfovibrio vulgaris (Dv) and the methanogenic archaeon Methanococcus maripaludis (Mm) unsustainable. By contrast, prolonged laboratory evolution in obligate syntrophy conditions improved the productivity of this community but at the expense of erosion of sulfate respiration (SR). Hence, we sought to understand the evolutionary trajectories that could both increase the productivity of syntrophic interactions and sustain SR. We combined a temporal and combinatorial survey of mutations accumulated over 1000 generations of 9 independently-evolved communities with analysis of the genotypic structure for one community down to the single-cell level. We discovered a high level of parallelism across communities despite considerable variance in their evolutionary trajectories and the perseverance of a rare SR+ Dv lineage within many evolution lines. An in-depth investigation revealed that synergistic epistasis across Dv and Mm genotypes had enhanced cooperativity within SR- and SR+ assemblages, allowing their co-existence as r- and K-strategists, respectively.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2020.06.22.160184DOIDiscussion Paper
https://github.com/sturkarslan/evolution-of-syntrophyRelated ItemData/Code
ORCID:
AuthorORCID
Turkarslan, Serdar0000-0003-1679-6405
Valenzuela, Jacob J.0000-0002-2320-241X
Hillesland, Kristina L.0000-0002-8779-7926
Additional Information: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-NC-ND 4.0 International license. This material by ENIGMA-Ecosystems and Networks Integrated with Genes and Molecular Assemblies (http://enigma.lbl.gov), a Science Focus Area Program at Lawrence Berkeley National Laboratory is based upon work supported by the U.S. Department of Energy, Office of Science, Office of Biological & Environmental Research under contract number DE-AC02-05CH11231. In addition, sequencing of ancestral cocultures and early generation samples was supported by the National Science Foundation under Grant No. DEB-1453205 and DEB-1257525 to KLH. The pipeline for sequencing data analysis was developed using funds from the National Institute of Health under grant number R01AI141953 to NSB. We would like to thank Nicholas Elliott for his help with growth analysis, Joseph Hellerstein, and Adrian Lopez Garcia de Lomana for discussion on data analysis. Author Contributions: Conceptualization and Methodology, S.T., N.S., N.S.B., D.A.S. and K.L.H; Investigation, S.T., N.S., A.W.T., C.E.A., J.J.V., J.W., K.A.H., J.H., Y.F., L.W., and Y.M.S.; Formal Analysis, S.T., N.S., and N.S.B.; Data Curation, S.T., N.S., K.L.H., K.A.H., and N.S.B; Writing – Original Draft, S.T., N.S.B., K.L.H., and D.A.S.; Visualization, S.T., N.S.B.; Supervision, N.S.B., K.L.H., and D.A.S.; Resources and Funding Acquisition, J.Z., N.S.B., K.L.H., and D.A.S. The authors have declared no competing interest. Data and Code Availability: Bulk and Single cell sequencing data used in this study and associated biosample meta-data information can be obtained through the NCBI Bioproject database (https://www.ncbi.nlm.nih.gov/bioproject) with accession number PRJNA248017. Custom R and Python codes used for sequence analysis, variant calling, data analysis and figure preparations are available on GitHub (https://github.com/sturkarslan/evolution-of-syntrophy). Annotated mutations within the context of other functional and regulatory genome information can be explored through Syntrophy Portal (http://networks.systemsbiology.net/syntrophy/).
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-AC02-05CH11231
NSFDEB-1453205
NSFDEB-1257525
NIHR01AI141953
Record Number:CaltechAUTHORS:20200626-103612993
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200626-103612993
Official Citation:Synergistic epistasis enhances cooperativity of mutualistic interspecies interactions Serdar Turkarslan, Nejc Stopnisek, Anne W Thompson, Christina E Arens, Jacob J Valenzuela, James Wilson, Kristopher A Hunt, Jessica Hardwicke, Sujung Lim, Yee Mey Seah, Ying Fu, Liyou Wu, Jizhong Zhou, Kristina L Hillesland, David A Stahl, Nitin S Baliga bioRxiv 2020.06.22.160184; doi: https://doi.org/10.1101/2020.06.22.160184
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104077
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:26 Jun 2020 19:48
Last Modified:26 Jun 2020 19:48

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