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Biogeography of American Northwest Hot Spring A/B′-Lineage Synechococcus Populations

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Biogeography of American Northwest Hot Spring A/B′-Lineage Synechococcus Populations ORIGINAL RESEARCH published: 24 February 2020 doi: 10.3389/fmicb.2020.00077 Biogeography of American Northwest Hot Spring A/B′-Lineage Synechococcus Populations Eric D. Becraft 1,2*†, Jason M. Wood 1,3†, Frederick M. Cohan 4 and David M. Ward 1 1 Department of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT, United States, 2 Department of Biology, University of North Alabama, Florence, AL, United States, 3 Biotechnology and Planetary Protection Group, Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA, United States, 4 Department of Biology, Wesleyan University, Middletown, CT, United States Previous analyses have shown how diversity among unicellular cyanobacteria inhabiting island-like hot springs is structured relative to physical separation and physiochemical Edited by: Haiwei Luo, differences among springs, especially at local to regional scales. However, these studies The Chinese University of have been limited by the low resolution provided by the molecular markers surveyed. We Hong Kong, China analyzed large datasets obtained by high-throughput sequencing of a segment of the Reviewed by: photosynthesis gene psaA from samples collected in hot springs from geothermal basins Alexander Bennett Chase, University of California, San Diego, in Yellowstone National Park, Montana, and Oregon, all known from previous studies to United States contain populations of A/B′-lineage Synechococcus. The fraction of identical sequences Cheryl P. Andam, < University of New Hampshire, was greater among springs separated by 50 km than among springs separated by United States >50 km, and springs separated by >800 km shared sequence variants only rarely. *Correspondence: Phylogenetic analyses provided evidence for endemic lineages that could be related Eric D. Becraft to geographic isolation and/or geochemical differences on regional scales. Ecotype [email protected] Simulation 2 was used to predict putative ecotypes (ecologically distinct populations), † These authors have contributed and their membership, and canonical correspondence analysis was used to examine equally to this work the geographical and geochemical bases for variation in their distribution. Across Specialty section: the range of Oregon and Yellowstone, geographical separation explained the largest This article was submitted to percentage of the differences in distribution of ecotypes (9.5% correlated to longitude; Evolutionary and Genomic Microbiology, 9.4% to latitude), with geochemical differences explaining the largest percentage of a section of the journal the remaining differences in distribution (7.4–9.3% correlated to magnesium, sulfate, Frontiers in Microbiology and sulfide). Among samples within the Greater Yellowstone Ecosystem, geochemical Received: 22 October 2019 differences significantly explained the distribution of ecotypes (6.5–9.3% correlated to Accepted: 15 January 2020 Published: 24 February 2020 magnesium, boron, sulfate, silicon dioxide, chloride, and pH). Nevertheless, differences Citation: in the abundance and membership of ecotypes in Yellowstone springs with similar Becraft ED, Wood JM, Cohan FM and chemistry suggested that allopatry may be involved even at local scales. Synechococcus Ward DM (2020) Biogeography of American Northwest Hot Spring populations have diverged both by physical isolation and physiochemical differences, and A/B′-Lineage Synechococcus populations on surprisingly local scales have been evolving independently. Populations. Front. Microbiol. 11:77. doi: 10.3389/fmicb.2020.00077 Keywords: ecotype, microbial species, population genetics, thermophilic Synechococcus, biogeography Frontiers in Microbiology | www.frontiersin.org 1 February 2020 | Volume 11 | Article 77 Becraft et al. Biogeography of American Northwest Synechococcus INTRODUCTION dispersal limitations in their biogeography (Castenholz, 1978, 1996). Hot spring microbial mats have been used as model systems to Molecular technologies have allowed many researchers to demonstrate ecological diversification by sympatric adaptation infer a role for dispersal limitation in generating biogeographic to parameters that vary along well-established environmental patterns of microbes (Johnson et al., 2006; Martiny et al., 2006; gradients (Ward et al., 2012). For instance, a progression of Chase et al., 2018). Pathogenic and symbiotic microorganisms unicellular cyanobacterial (Synechococcus) 16S rRNA genotypes that are associated with specific eukaryotic hosts have been ′′ ′ ′ (A ,A ,A,B , and B, respectively) can be found along a thermal shown to be restricted to the geographic range of their hosts gradient in alkaline siliceous hot springs in Yellowstone National (Falush et al., 2003; Taylor et al., 2005; Peay et al., 2010). Park (YNP) (Ferris and Ward, 1997). This patterning led to the Geographic barriers have also been shown to isolate populations hypothesis that closely related Synechococcus populations might of hyperthemophilic Archaea (Whitaker et al., 2003; Whitaker, have different temperature adaptations and this was confirmed 2006). Likewise, thermophilic Synechococcus populations have for isolates representative of these genotypes (Allewalt et al., been shown to be differentiated by geography (Ward and 2006). Greater molecular resolution provided by a portion Castenholz, 2002; Papke et al., 2003; Ward et al., 2012). These of the gene encoding a major photosystem I reaction center studies provided evidence that geographic isolation has been an protein (psaA locus) demonstrated the existence of more closely important factor in the diversification of microbial populations. related clades that were masked within 16S rRNA defined In the case of hot spring Synechococcus populations, Papke genotypes. These clades were shown to be ecologically distinct et al. (2003) showed that different Synechococcus 16S rRNA through their associations with different light environments at genotypes were predominant in Japanese, New Zealand and different depths in the upper 1 mm in these mats (Becraft North American hot springs and were only rarely shared among et al., 2015). Isolates representative of psaA genotypes uniquely springs in these locations. Analysis of the more rapidly evolving distributed along the vertical aspect of the mat were differently 16S-23S rRNA internal transcribed spacer region suggested adapted to light intensity and quality (Nowack et al., 2015) regional variation in community members within Japanese and showed differences in gene content that may explain why and North American hot springs of different thermal basins, these adaptations were observed (Olsen et al., 2015). In studies even in springs with very similar chemistry. Papke et al. based on psaA variation, sequence clusters were demarcated (2003) characterized diversity using cloning and sequencing into ecologically distinct populations (ecotypes) based on the methods, so the sampling was limited. Furthermore, these Stable Ecotype model of species and speciation. Here, the genetic markers have been shown to be too slowly evolving Ecotype Simulation algorithm identified sympatric ecotypes to distinguish the most newly divergent ecological species (or satisfying the criteria for defining ecological species: they were ecotypes) of Synechococcus (Becraft et al., 2011, 2015; Melendrez ecologically distinct from one another and they were each et al., 2011). Additionally, these studies did not quantify how ecologically homogeneous. diversity within each hot spring was influenced by differences Because hot springs resemble islands, they also present an in the environmental parameters measured. These issues limit opportunity to understand the role of allopatric processes (i.e., our ability to fully understand the relationship between local physical isolation) in diversification of microbial populations and regional communities, and thus the roles of dispersal (Papke et al., 2003). For many years, it was widely believed and allopatric and sympatric processes in diversification of that barriers to the distribution of microbial species did not Synechococcus species. exist, and that “everything is everywhere, and the environment In this study, we reanalyzed American Northwest samples selects” (Baas Becking, 1934). In essence, microorganisms were collected by Papke et al. (2003) using high-throughput thought to primarily evolve through sympatric means, and to sequencing of amplicons of a segment of a more highly- be distributed globally without geographical barriers limiting resolving, protein-encoding locus (psaA) (Becraft et al., 2011, their dispersal. Observations leading to such inferences were 2015). We have used Ecotype Simulation 2 (Wood et al., often based on a low-resolution taxonomy such as morphology 2020) to identify the most newly divergent psaA segment (Finlay and Fenchel, 2004). However, morphology is often a sequence clusters that can coexist indefinitely because they poor indicator of species richness and can mask the genetic and are either ecologically distinct (ecotypes) or geographically ecological diversity that exists in nature. It can be challenging isolated populations (geotypes), or both (Cohan and Perry, to study the spatial dynamics of microbial populations at 2007). This permitted rigorous analysis of the distribution of large scale because (i) evolutionarily distinct organisms can A- and B′-like Synechococcus genetic diversity in hot springs share similar morphologies, (ii) cultivated organisms are not that are separated by <1 to > 800 km, with the aim of
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