Continental-Scale Gene Flow Prevents Allopatric Divergence of Pelagic Freshwater Bacteria

Abstract

Allopatric divergence is one of the principal mechanisms for speciation of macro-organisms. Microbes by comparison are assumed to disperse more freely and to be less limited by dispersal barriers. However, thermophilic prokaryotes restricted to geothermal springs have shown clear signals of geographic isolation, but robust studies on this topic for microbes with less strict habitat requirements are scarce. Furthermore, it has only recently been recognized that homologous recombination among conspecific individuals provides species coherence in a wide range of prokaryotes. Recombination barriers thus may define prokaryotic species boundaries, yet, the extent to which geographic distance between populations gives rise to such barriers is an open question. Here, we investigated gene flow and population structure in a widespread species of pelagic freshwater bacteria, Polynucleobacter paneuropaeus. Through comparative genomics of 113 conspecific strains isolated from freshwater lakes and ponds located across a North-South range of more than 3000 km, we were able to reconstruct past gene flow events. The species turned out to be highly recombinogenic as indicated by significant signs of gene transfer and extensive genome mosaicism. While genomic differences increased with spatial distance on a regional scale (< 170 km), such correlations were mostly absent on larger scales up to 3400 km. We conclude that allopatric divergence in European P. paneuropaeus is minor, and that effective gene flow across the sampled geographic range in combination with a high recombination efficacy maintains species coherence.

Opening a next‐generation black box: Ecological trends for hundreds of species‐like taxa uncovered within a single bacterial >99% 16S rRNA operational taxonomic unit

“…Partial Mantel tests controlling for environmental influences did not suggest that dissimilarity of Polynucleobacter communities increased with geographic distance (Table S3). This was in line with a recent study on population structure of P. paneuropaeus along the same South-North range studied here, which suggested a lack of dispersal barriers along this 3,400 km latitudinal range (Hoetzinger et al, 2021). The detection of OTUs exclusively found in only one of the three investigated regions (Figure 7b) is well explained by the abundance-occupancy relationship documented in macroecology (Gaston et al, 2000), which predicts a positive relationship between the abundance of a taxon and its range occupancy (Figure 7c).…”

Partners in space: Discordant population structure between legume hosts and rhizobium symbionts in their native range

“…It is this population scale that is most relevant to local adaptation and coevolution (Thompson 2005;Hoeksema and Forde 2008;Kraemer and Boynton 2017). Like other diverse microbial systems (Vos and Velicer 2008;Chase et al 2019;Hoetzinger et al 2021), Ensifer displays both isolation by distance (chromosome) and population genetic structure (all elements); nevertheless, we found extremely closely-related strains up to 1350 km apart -indicating at least some long-distance dispersal.…”

“…Based on metagenomics datasets, rhizobia have many characteristics associated with large geographic ranges and, by extension, large dispersal ability (e.g., being Proteobacteria, plantassociated or soil-borne taxa, and large genome sizes; Choudoir et al 2018). However, metagenomic studies of microbial communities are limited in their resolution; therefore, population genomic data (Hoetzinger et al 2021), coupled with spatially-structured samples of both within-and among-population variation (Whitaker and Banfield 2006), are required for inferring population-level processes such as gene flow. It is this population scale that is most relevant to local adaptation and coevolution (Thompson 2005;Hoeksema and Forde 2008;Kraemer and Boynton 2017).…”

“…Based on metagenomics datasets, rhizobia have many characteristics associated with large geographic ranges and, by extension, large dispersal ability (e.g., Proteobacteria, plant-associated or soil-borne taxa, and large genome sizes; Choudoir et al 2018). However, metagenomic studies of microbial communities are limited in their resolution; therefore, population genomic data (Hoetzinger, Pitt, Huemer, & Hahn, 2021), coupled with spatially-structured samples of both within-and among-population variation (Whitaker & Banfield, 2006), are required for inferring population structure and gene flow, which are key to local adaptation and coevolution (Thompson 2005;Hoeksema and Forde 2008;Kraemer and Boynton 2017). Like other diverse microbial systems (Chase et al, 2019;Hoetzinger et al, 2021;Vos & Velicer, 2008), Ensifer displays both isolation by distance (chromosome) and population genetic structure (all elements); nevertheless, we found extremely closely-related strains up to 1350 km apart -indicating at least some long-distance dispersal.…”

“…However, metagenomic studies of microbial communities are limited in their resolution; therefore, population genomic data (Hoetzinger, Pitt, Huemer, & Hahn, 2021), coupled with spatially-structured samples of both within-and among-population variation (Whitaker & Banfield, 2006), are required for inferring population structure and gene flow, which are key to local adaptation and coevolution (Thompson 2005;Hoeksema and Forde 2008;Kraemer and Boynton 2017). Like other diverse microbial systems (Chase et al, 2019;Hoetzinger et al, 2021;Vos & Velicer, 2008), Ensifer displays both isolation by distance (chromosome) and population genetic structure (all elements); nevertheless, we found extremely closely-related strains up to 1350 km apart -indicating at least some long-distance dispersal. Large dispersal ability, together with the observation of abundant local phenotypic (Heath, 2010;Heath & Tiffin, 2009) and genomic (Bailly et al, 2011;Bailly, Olivieri, De Mita, Cleyet-Marel, & Béna, 2006) variation for symbiosis, suggests that most of the variation relevant to both bacterial adaptation and coevolution can be found at relatively small spatial scales.…”