Evolution of population structure and genomic diversity

Because horizontal gene transfer is common among microbes, species concepts developed for sexual eukaryotes have not been applicable to these organisms. One of the most puzzling observations is that individuals (clones), which are nearly identical in most of their genes, can have hundreds of genes that are differentially present or absent in their genomes. Our population model has yielded important insights into how populations differentiate in light of environmental selection and maintain such genomic diversity even during speciation events. A major breakthrough was the detailed genomic analysis of two recently speciated populations, that already showed differential ecological specialization. Counter to the most commonly cited model, which predicted genome-wide sweeps, we showed that genes can sweep in a population specific manner, i.e., akin to sexual eukaryotes where recombination allows high rates of gene flow. The observed ecological differentiation was accompanied by a competition-dispersal tradeoff as a potential explanation for microscale separation of gene pools during early speciation. Our population model has also allowed us to make progress in explaining gene content diversity within members of populations. For example, we have observed that cheater phenotypes often differ in gene content (rather than regulation) in public good dynamics. We are currently finding similar results in predator-prey interactions so that we are able to provide a more general understanding on how environmental selection causes such large gene content variation across closely related genomes.


Selected references:

Shapiro, B.J., Friedman, J., Cordero, O.X., Preheim, S.P., Timberlake, S.C., Szabo, G., Polz&, M.F., Alm&, E.J. (2012) Population genomics of early events in the ecological differentiation of bacteria. Science 336:48-51. (& co-last authors)

Cordero*, O.X., Wildschutte*, H., Kirkup*, B., Proehl, S., Ngo, L., Hussain, F., Le Roux, F., Mincer, T., Polz, M.F. (2012) Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance. Science. 337:1228-1231.

Cordero, O.X., Ventouras, L.-A., DeLong, E.F., Polz, M.F. (2012) Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations.  Proc. Natl. Acad. Sci. USA. 109(49):20059-20064.

Yawata, Y., Cordero, O.X., Menolascina, F., Hehemann, J.-H., Polz, M.F., Stocker, R. (2014) A competition dispersal trade-off ecologically differentiates recently speciated marine bacterioplankton populations.  Proc. Natl. Acad. Sci. USA. 111(15):5622-5627.

Hehemann, J.-H., Arevalo, P., Datta, M.S., Yu, A., Corzett, C., Henschel, A., Preheim, S.P., Timberlake, S., Alm, E.J., Polz, M.F. (2016) Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes. Nature Comm. 7:12860

Arevalo, P. VanInsberghe, D., Elsherbini, J., Gore, J., Polz, M.F. (2019) A reverse ecology approach based on a biological definition of microbial populations. Cell 178(4):820-834.e14