Differential Functional Constraints Cause Strain-Level Endemism inPolynucleobacterPopulations.
The adaptation of bacterial lineages to local environmental conditions creates the potential for broader genotypic diversity within a species, which can enable a species to dominate across ecological gradients because of niche flexibility. The genusPolynucleobactermaintains both free-living and symbiotic ecotypes and maintains an apparently ubiquitous distribution in freshwater ecosystems. Subspecies-level resolution supplemented with metagenome-derived genotype analysis revealed that differential functional constraints, not geographic distance, produce and maintain strain-level genetic conservation inPolynucleobacterpopulations across three geographically proximal riverine environments. Genes associated with cofactor biosynthesis and one-carbon metabolism showed habitat specificity, and protein-coding genes of unknown function and membrane transport proteins were under positive selection across each habitat. Characterized by different median ratios of nonsynonymous to synonymous evolutionary changes (dN/dSratios) and a limited but statistically significant negative correlation between thedN/dSratio and codon usage bias between habitats, the free-living and core genotypes were observed to be evolving under strong purifying selection pressure. Highlighting the potential role of genetic adaptation to the local environment, the two-component system protein-coding genes were highly stable (dN/dSratio, < 0.03). These results suggest that despite the impact of the habitat on genetic diversity, and hence niche partition, strong environmental selection pressure maintains a conserved core genome forPolynucleobacterpopulations.IMPORTANCEUnderstanding the biological factors influencing habitat-wide genetic endemism is important for explaining observed biogeographic patterns.Polynucleobacteris a genus of bacteria that seems to have found a way to colonize myriad freshwater ecosystems and by doing so has become one of the most abundant bacteria in these environments. We sequenced metagenomes from locations across the Chicago River system and assembledPolynucleobactergenomes from different sites and compared how the nucleotide composition, gene codon usage, and the ratio of synonymous (codes for the same amino acid) to nonsynonymous (codes for a different amino acid) mutations varied across these population genomes at each site. The environmental pressures at each site drove purifying selection for functional traits that maintained a streamlined core genome across the Chicago RiverPolynucleobacterpopulation while allowing for site-specific genomic adaptation. These adaptations enablePolynucleobacterto become dominant across different riverine environmental gradients.
Biosciences Division, Argonne National Laboratory, Lemont, Illinois, USA; Department of Surgery and Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, USA.
Naseer
N
Sangwan
Biosciences Division, Argonne National Laboratory, Lemont, Illinois, USA.
Iratxe
I
Zarraonaindia
Biosciences Division, Argonne National Laboratory, Lemont, Illinois, USA; Department of Surgery and Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, USA.
Jarrad T
JT
Hampton-Marcell
Energy Systems Division, Argonne National Laboratory, Lemont, Illinois, USA.
Herbert
H
Ssegane
Biosciences Division, Argonne National Laboratory, Lemont, Illinois, USA.
Tifani W
TW
Eshoo
Metropolitan Water Reclamation District of Greater Chicago, Cicero, Illinois, USA.
Geeta
G
Rijal
Energy Systems Division, Argonne National Laboratory, Lemont, Illinois, USA.
M Cristina
MC
Negri
Biosciences Division, Argonne National Laboratory, Lemont, Illinois, USA; Department of Surgery and Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, USA.
Jack A
JA
Gilbert
metagenomics