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Horizontal Transmission and Recombination Maintain Forever Young Bacterial Symbiont Genomes

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Horizontal Transmission and Recombination Maintain Forever Young Bacterial Symbiont Genomes University of Rhode Island DigitalCommons@URI Graduate School of Oceanography Faculty Publications Graduate School of Oceanography 2020 Horizontal Transmission and Recombination Maintain forever Young Bacterial Symbiont Genomes Shelbi Russell Evan Pepper-Tunick Jesper Svedberg Svedberg Ashley Byrne Jennie Ruelas Castillo See next page for additional authors Follow this and additional works at: https://digitalcommons.uri.edu/gsofacpubs Citation/Publisher Attribution Russell SL, Pepper-Tunick E, Svedberg J, Byrne A, Ruelas Castillo J, Vollmers C, et al. (2020) Horizontal transmission and recombination maintain forever young bacterial symbiont genomes. PLoS Genet 16(8): e1008935. https://doi.org/10.1371/journal.pgen.1008935 This Article is brought to you for free and open access by the Graduate School of Oceanography at DigitalCommons@URI. It has been accepted for inclusion in Graduate School of Oceanography Faculty Publications by an authorized administrator of DigitalCommons@URI. For more information, please contact [email protected]. Authors Shelbi Russell, Evan Pepper-Tunick, Jesper Svedberg Svedberg, Ashley Byrne, Jennie Ruelas Castillo, Christopher Vollmers, Roxanne A. Beinart, and Russell Corbett-Detig This article is available at DigitalCommons@URI: https://digitalcommons.uri.edu/gsofacpubs/724 PLOS GENETICS RESEARCH ARTICLE Horizontal transmission and recombination maintain forever young bacterial symbiont genomes 1,2 2,3 2,3 1 Shelbi L. RussellID *, Evan Pepper-TunickID , Jesper SvedbergID , Ashley ByrneID , 1 2,3 4 Jennie Ruelas CastilloID , Christopher Vollmers , Roxanne A. BeinartID , 2,3 Russell Corbett-DetigID * 1 Department of Molecular Cellular and Developmental Biology. University of California Santa Cruz, Santa Cruz, California, United States of America, 2 Department of Biomolecular Engineering. University of a1111111111 California Santa Cruz, Santa Cruz, California, United States of America, 3 Genomics Institute, University of a1111111111 California, Santa Cruz, California, United States of America, 4 Graduate School of Oceanography. University a1111111111 of Rhode Island, Narragansett, Rhode Island, United States of America a1111111111 a1111111111 * [email protected] (SLR); [email protected] (RCD) Abstract OPEN ACCESS Bacterial symbionts bring a wealth of functions to the associations they participate in, but by Citation: Russell SL, Pepper-Tunick E, Svedberg J, doing so, they endanger the genes and genomes underlying these abilities. When bacterial Byrne A, Ruelas Castillo J, Vollmers C, et al. (2020) symbionts become obligately associated with their hosts, their genomes are thought to Horizontal transmission and recombination decay towards an organelle-like fate due to decreased homologous recombination and inef- maintain forever young bacterial symbiont genomes. PLoS Genet 16(8): e1008935. https:// ficient selection. However, numerous associations exist that counter these expectations, doi.org/10.1371/journal.pgen.1008935 especially in marine environments, possibly due to ongoing horizontal gene flow. Despite Editor: Xavier Didelot, University of Warwick, extensive theoretical treatment, no empirical study thus far has connected these underlying UNITED KINGDOM population genetic processes with long-term evolutionary outcomes. By sampling marine Received: November 10, 2019 chemosynthetic bacterial-bivalve endosymbioses that range from primarily vertical to strictly horizontal transmission, we tested this canonical theory. We found that transmission mode Accepted: June 16, 2020 strongly predicts homologous recombination rates, and that exceedingly low recombination Published: August 25, 2020 rates are associated with moderate genome degradation in the marine symbionts with Peer Review History: PLOS recognizes the nearly strict vertical transmission. Nonetheless, even the most degraded marine endosym- benefits of transparency in the peer review biont genomes are occasionally horizontally transmitted and are much larger than their ter- process; therefore, we enable the publication of all of the content of peer review and author restrial insect symbiont counterparts. Therefore, horizontal transmission and recombination responses alongside final, published articles. The enable efficient natural selection to maintain intermediate symbiont genome sizes and sub- editorial history of this article is available here: stantial functional genetic variation. https://doi.org/10.1371/journal.pgen.1008935 Copyright: © 2020 Russell et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and Author summary reproduction in any medium, provided the original Symbiotic associations between bacteria and eukaryotes are ubiquitous in nature and have author and source are credited. contributed to the evolution of radically novel phenotypes and niches for the involved Data Availability Statement: Data and genome partners. New metabolic or physiological capacities that arise in these associations are typ- assemblies generated in this study are available ically encoded by the bacterial symbiont genomes. However, the association itself endan- through NCBI BioProject number PRJNA562081 (BioSample numbers listed in S1 Table). Code gers the retention of bacterial genomic coding capacity. Endosymbiont genome evolution PLOS Genetics | https://doi.org/10.1371/journal.pgen.1008935 August 25, 2020 1 / 27 PLOS GENETICS Forever young bacterial symbiont genomes written and used in our analyses is available from https://github.com/shelbirussell/ theory predicts that when bacterial symbionts become restricted to host tissues, their pop- ForeverYoungGenomes_Russell-et-al. Underlying ulations cannot remove deleterious mutations efficiently. This ultimately results in their numerical data for all graphs and summary genomes degrading to small, function-poor states, reminiscent of organellar genomes. statistics are available as Supporting Information. However, many ancient marine endosymbionts do not fit this prediction, but instead Funding: This work was supported by UC Santa retain relatively large, gene-rich genomes, indicating that the evolutionary dynamics of Cruz, Harvard University, the Alfred P. Sloan this process need more thorough characterization. Here we show that on-going symbiont Foundation (to RCD; sloan.org), and the NIH (R35GM128932 to RCD; nih.gov). Funding for Lau gene flow via horizontal transmission between bivalve hosts and recombination among Basin collections was provided by the Schmidt divergent gammaproteobacterial symbiont lineages are sufficient to maintain large and Ocean Institute and NSF (OCE-1819530 to RB; nsf. dynamic bacterial symbiont genomes. These findings indicate that many obligately associ- gov), Funding for the Veatch Canyon collection was ated symbiont genomes may not be as isolated from one another as previously assumed provided via a UNOLS Early Career Training Cruise and are not on a one way path to degradation. Program funded by the NSF (OCE-1641453, OCE- 1638805, OCE-1214335, OCE- 1655587, and OCE- 1649756; nsf.gov) and the ONR (N00014±15-1± 2583; onr.navy.mil). The funders had no role in study design, data collection and analysis, decision Introduction to publish, or preparation of the manuscript. Bacterial genomes encode an enormous diversity of functions, which enable them to create Competing interests: The authors have declared radically novel phenotypes when they associate with eukaryotic hosts. However, they are at that no competing interests exist. risk of genome degradation and function loss within these associations. Among the diversity of eukaryotic hosts they inhabit, symbiont genome sizes range from nearly unreduced genomes that are similar to their free-living relatives (~3±5 Mb) to highly reduced genomes that are less than 10% of the size of their free-living ancestors (~0.2±0.6 Mb) [1,2]. The degra- dation process often leaves genes required for the bacterium's role in the symbiosis, and removes seemingly vital genes, such as those involved in DNA repair and replication [1]. Although genome erosion may be enabled in some cases due to ªstreamliningº benefits [3], it is clear that the process can become problematic and can ultimately result in symbiont replace- ment or supplementation [1,4] to accomplish the full repertoire of functions needed in the combined organism. Thus, to fully understand how symbioses evolve, we must first under- stand the pressures their genomes experience. Symbiont genome evolution theory predicts that upon host restriction, bacterial genomes begin the steady and inexorable process of decay due to decreased population sizes and homol- ogous recombination rates, which result in inefficacious natural selection [5]. The transmis- sion bottleneck that occurs when symbionts are passed on to host offspring further exacerbates these dynamics by making deleterious mutations more likely to drift to fixation in the next generation [5,6]. Indeed, many endosymbiont taxa exhibit weak purifying selection at the gene level [7±10]. In the early stages of bacterial symbiont-host associations, deleterious mutations arise on each symbiont chromosome and a portion drift or hitchhike with adaptive mutations to fixation. Subsequently, pseudogenes are lost entirely via deletion [5]. Ultimately, this process is thought to result in an organelle-like genome that is a fraction of the size of its free-living ancestors and has relegated many of its core cellular functions (e.g.,
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