Evolutionary history, processes, and mechanisms of ecologically important microbial lineages

We are interested in the microbial evolution and genomic changes in the context of the evolutionary history of their habitats. To address questions in this area, we work on high-quality genome sequences of phylogenetically and ecologically diverse lineages within a microbial group of interest, and employ molecular dating approaches, unbiased phylogenomic strategies, metagenome binning methods, single cell genomics, genome-scale metabolic modeling and individual-based modeling among other computational approaches. We also use and develop methods to probe the neutral and selective mechanisms underlying the genomic changes, which helps understand the genome size and genomic base composition variations within a lineage.

Here are a few recent examples of microbial evolutionary history studies. (1) We developed a fossil-independent molecular dating method based on the unbiased spontaneous mutation rate and subsequently estimated the evolutionary time of the Roseobacter group, the most abundant bacterial lineage in the coastal environments and a major player in marine carbon and sulfur cycles (Sun et al. 2017. The ISME Journal). (2) In a study of Flavobacteriaceae, one of the major bacterial groups responsible for global polysaccharide and peptide degradation, we predicted three major ocean-to-land transitions in their evolutionary history, which were associated with repeated losses of marine signature genes and repeated gains of non-marine adaptive genes (Zhang et al. 2019. Environmental Microbiology). (3) Thaumarchaeota, an archaeal group known to drive ammonia oxidation in both marine and terrestrial environments, experienced an ancient innovation in the terrestrial habitats from the non-ammonia-oxidizing ancestors to the ammonia-oxidizing descendants, followed by expansions to the photic shallow ocean and then to the dark deep ocean. We showed that these transitions were associated with substantial changes in the metabolic potentials, and predicted that the timing of these transitions matches well with the oxygenation events on these major habitats (Ren et al. 2019. The ISME Journal).

In the case of evolutionary mechanisms, we provided strong evidence for random genetic drift as the dominant evolutionary mechanism driving genome reduction of marine Prochlorococcus and the SAR86 clade and challenged the Darwin’s theory in explaining this prevalent phenomenon in the ocean (Luo et al. 2017. Nature Microbiology). In another study, we constructed a genome-scale individual-based model for a representative Roseobacter strain, which is parameterized by experimentally determined mutation and physiological data. We reached a conclusion that the neutral mutational bias is not sufficient to give rise to the observed genomic G+C content of this bacterium and that carbon limitation has been the primary selective force driving the G+C content of this bacterium since the origin of the Roseobacter group (Hellweger et al. 2018. The ISME Journal). This study also showed that the genomic G+C content is a window for looking into the past of the ocean chemistry, which complements the available geochemical measurements of the paleo-ocean chemistry.

Microevolution of ecologically important bacterial lineages

More recently, we become interested in microbial microevolution in the context of environmental heterogeneity at the local and global scales. A few interesting directions we are heading include microbial processes leading to coherence of seemingly separated populations, genomic mechanisms and environmental processes leading to population differentiation and microbial speciation, dispersal limitation and biogeography of microbial populations. We integrate well-designed field sampling, high-throughput microbial cultivation, large-scale genomic analyses, and bioinformatics-guided experimental assays to address these questions.

We are particularly interested in the Roseobacter group, Flavobacteriaceae, and plant-associated rhizobia and their free-living relatives in the soil. They are metabolically versatile and dominate the microbial communities in a variety of natural habitats. Importantly, these bacteria often readily grow on solid media, making it possible to collect pure cultures in a high-throughput way. We have been developing novel cultivation pipelines and building culture collections of these bacterial groups from diverse environments for microevolution studies.