skip to main content


Title: Microcoleus (Cyanobacteria) form watershed‐wide populations without strong gradients in population structure
Abstract

The relative importance of separation by distance and by environment to population genetic diversity can be conveniently tested in river networks, where these two drivers are often independently distributed over space. To evaluate the importance of dispersal and environmental conditions in shaping microbial population structures, we performed genome‐resolved metagenomic analyses of benthicMicrocoleus‐dominated cyanobacterial mats collected in the Eel and Russian River networks (California, USA). The 64 Microcoleusgenomes were clustered into three species that shared >96.5% average nucleotide identity (ANI). Most mats were dominated by one strain, but minor alleles within mats were often shared, even over large spatial distances (>300 km). Within the most commonMicrocoleusspecies, the ANI between the dominant strains within mats decreased with increasing spatial separation. However, over shorter spatial distances (tens of kilometres), mats from different subwatersheds had lower ANI than mats from the same subwatershed, suggesting that at shorter spatial distances environmental differences between subwatersheds in factors like canopy cover, conductivity, and mean annual temperature decreases ANI. Since mats in smaller creeks had similar levels of nucleotide diversity (π) as mats in larger downstream subwatersheds, within‐mat genetic diversity does not appear to depend on the downstream accumulation of upstream‐derived strains. The four‐gamete test and sequence length bias suggest recombination occurs between almost all strains within each species, even between populations separated by large distances or living in different habitats. Overall, our results show that, despite some isolation by distance and environmental conditions, sufficient gene‐flow occurs among cyanobacterial strains to prevent either driver from producing distinctive population structures across the watershed.

 
more » « less
Award ID(s):
1656009 1331940
NSF-PAR ID:
10445859
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
31
Issue:
1
ISSN:
0962-1083
Page Range / eLocation ID:
p. 86-103
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Blooms of planktonic cyanobacteria have long been of concern in lakes, but more recently, harmful impacts of riverine benthic cyanobacterial mats been recognized. As yet, we know little about how various benthic cyanobacteria are distributed in river networks, or how environmental conditions or other associated microbes in their consortia affect their biosynthetic capacities. We performed metagenomic sequencing for 22 Oscillatoriales-dominated (Cyanobacteria) microbial mats collected across the Eel River network in Northern California and investigated factors associated with anatoxin-a producing cyanobacteria. All microbial communities were dominated by one or two cyanobacterial species, so the key mat metabolisms involve oxygenic photosynthesis and carbon oxidation. Only a few metabolisms fueled the growth of the mat communities, with little evidence for anaerobic metabolic pathways. We genomically defined four cyanobacterial species, all which shared <96% average nucleotide identity with reference Oscillatoriales genomes and are potentially novel species in the genus Microcoleus. One of the Microcoleus species contained the anatoxin-a biosynthesis genes, and we describe the first anatoxin-a gene cluster from the Microcoleus clade within Oscillatoriales. Occurrence of these four Microcoleus species in the watershed was correlated with total dissolved nitrogen and phosphorus concentrations, and the species that contains the anatoxin-a gene cluster was found in sites with higher nitrogen concentrations. Microbial assemblages in mat samples with the anatoxin-a gene cluster consistently had a lower abundance of Burkholderiales (Betaproteobacteria) species than did mats without the anatoxin-producing genes. The associations of water nutrient concentrations and certain co-occurring microbes with anatoxin-a producing Microcoleus motivate further exploration for their roles as potential controls on the distributions of toxigenic benthic cyanobacteria in river networks. 
    more » « less
  2. Abstract

    Blooms of planktonic cyanobacteria have long been of concern in lakes, but more recently, harmful impacts of riverine benthic cyanobacterial mats been recognized. As yet, we know little about how various benthic cyanobacteria are distributed in river networks, or how environmental conditions or other associated microbes in their consortia affect their biosynthetic capacities. We performed metagenomic sequencing for 22 Oscillatoriales-dominated (Cyanobacteria) microbial mats collected across the Eel River network in Northern California and investigated factors associated with anatoxin-a producing cyanobacteria. All microbial communities were dominated by one or two cyanobacterial species, so the key mat metabolisms involve oxygenic photosynthesis and carbon oxidation. Only a few metabolisms fueled the growth of the mat communities, with little evidence for anaerobic metabolic pathways. We genomically defined four cyanobacterial species, all which shared <96% average nucleotide identity with reference Oscillatoriales genomes and are potentially novel species in the genus Microcoleus. One of the Microcoleus species contained the anatoxin-a biosynthesis genes, and we describe the first anatoxin-a gene cluster from the Microcoleus clade within Oscillatoriales. Occurrence of these four Microcoleus species in the watershed was correlated with total dissolved nitrogen and phosphorus concentrations, and the species that contains the anatoxin-a gene cluster was found in sites with higher nitrogen concentrations. Microbial assemblages in mat samples with the anatoxin-a gene cluster consistently had a lower abundance of Burkholderiales (Betaproteobacteria) species than did mats without the anatoxin-producing genes. The associations of water nutrient concentrations and certain co-occurring microbes with anatoxin-a producing Microcoleus motivate further exploration for their roles as potential controls on the distributions of toxigenic benthic cyanobacteria in river networks.

     
    more » « less
  3. Abstract

    What a strain is and how many strains make up a natural bacterial population remain elusive concepts despite their apparent importance for assessing the role of intra-population diversity in disease emergence or response to environmental perturbations. To advance these concepts, we sequenced 138 randomly selectedSalinibacter ruberisolates from two solar salterns and assessed these genomes against companion short-read metagenomes from the same samples. The distribution of genome-aggregate average nucleotide identity (ANI) values among these isolates revealed a bimodal distribution, with four-fold lower occurrence of values between 99.2% and 99.8% relative to ANI >99.8% or <99.2%, revealing a natural “gap” in the sequence space within species. Accordingly, we used this ANI gap to define genomovars and a higher ANI value of >99.99% and shared gene-content >99.0% to define strains. Using these thresholds and extrapolating from how many metagenomic reads each genomovar uniquely recruited, we estimated that –although our 138 isolates represented about 80% of theSal. ruberpopulation– the total population in one saltern pond is composed of 5,500 to 11,000 genomovars, the great majority of which appear to be rare in-situ. These data also revealed that the most frequently recovered isolate in lab media was often not the most abundant genomovar in-situ, suggesting that cultivation biases are significant, even in cases that cultivation procedures are thought to be robust. The methodology and ANI thresholds outlined here should represent a useful guide for future microdiversity surveys of additional microbial species.

     
    more » « less
  4. Abstract Aim

    Current distributions of widespread North American (NA) species have been shaped by Pleistocene glacial cycles, latitudinal temperature gradients, sharp longitudinal habitat transitions and the vicariant effects of major mountain and river systems that subdivide the continent. Within these transcontinental species, genetic diversity patterns might not conform to established biogeographic breaks compared to more spatially restricted taxa due to intrinsic differences or spatiotemporal differences. In this study, we highlight the effects of these extrinsic variables on genetic structuring by investigating the phylogeographic history of a widespread generalist squamate found throughout NA.

    Location

    North America.

    Taxon

    Common gartersnake,Thamnophis sirtalis.

    Methods

    We evaluate the effects of major river basins and the forest‐grassland transition into the Interior Plains on genetic structure patterns using phylogenetic, spatially informed population structure and demographic analyses of single nucleotide polymorphism data and address range expansion history with ecological niche modelling using locality and historic climate data.

    Results

    We identify four phylogeographic lineages with varying degrees of connectivity between them. We find discordant population structure patterns between sex‐linked and autosomal loci with respect to the relationship between the central NA lineage relative to coastal lineages. We find support for southeast Pleistocene refugia where recent secondary contact occurred during the Last Glacial Maximum and evidence for both northern and southern refugia in western NA.

    Main Conclusion

    Our results provide strong evidence for a Pliocene origin forT. sirtalisin central‐southeastern NA preceding its rapid expansion across the continent prior to middle Pleistocene climate‐mediated lineage formation. We implicate major riverine networks within the Mississippi watershed in likely repeated westward expansion events across the Interior Plains. Finally, we corroborate prior conclusions that phenotypic differences between subspecies do not reflect shared evolutionary history and note that the degree of separation between inferred lineages warrants further investigation before any taxonomic revisions are proposed.

     
    more » « less
  5. Abstract

    Range expansions driven by global change and species invasions may have significant genomic, evolutionary, and ecological implications. During range expansions, strong genetic drift characterized by repeated founder events can result in decreased genetic diversity with increased distance from the center of the historic range, or the point of invasion. The invasion of the Indo‐Pacific lionfish,Pterois volitans, into waters off the US East Coast, Gulf of Mexico, and Caribbean Sea provides a natural system to study rapid range expansion in an invasive marine fish with high dispersal capabilities. We report results from 12,759 single nucleotide polymorphism loci sequenced by restriction enzyme‐associated DNA sequencing for nineP. volitanssampling areas in the invaded range, including Florida and other sites throughout the Caribbean, as well as mitochondrial control region D‐loop data. Analyses revealed low to no spatially explicit metapopulation genetic structure, which is partly consistent with previous finding of little structure within ocean basins, but partly divergent from initial reports of between‐basin structure. Genetic diversity, however, was not homogeneous across all sampled sites. Patterns of genetic diversity correlate with invasion pathway. Observed heterozygosity, averaged across all loci within a population, decreases with distance from Florida while expected heterozygosity is mostly constant in sampled populations, indicating population genetic disequilibrium correlated with distance from the point of invasion. Using anFSToutlier analysis and a Bayesian environmental correlation analysis, we identified 256 and 616 loci, respectively, that could be experiencing selection or genetic drift. Of these, 24 loci were shared between the two methods.

     
    more » « less