Evolutionary ecology of natural comammoxNitrospirapopulations

Abstract

Microbial life on Earth commonly occurs in diverse and complex communities where species interact, and their genomic repertoires evolve over time. Our understanding of species interaction and evolution has increased during last decades, but most studies of evolutionary dynamics are based on single species in isolation or experimental systems composed of few interacting species. Here, we use the microbial ecosystem found in groundwater-fed sand filters as a model to avoid this limitation. In these systems, diverse microbial communities experience relatively stable conditions, and the coupling between chemical and biological processes is generally well defined. Metagenomic analysis of 12 sand filters revealed systematic co-occurrence of at least five comammox Nitrospira species, favoured by low ammonium concentrations. Nitrospira species showed intra-population sequence diversity, although possible clonal expansion was detected in few abundant local comammox populations. Nitrospira populations were separated by gene flow boundaries, suggesting natural and cohesive populations. They showed low homologous recombination and strong purifying selection, the latest process being especially strong in genes essential in energy metabolism. Positive selection was detected on genes related to resistance to foreign DNA and phages. Additionally, we analysed evolutionary processes in populations from different habitats. Interestingly, our results suggest that in comammox Nitrospira these processes are not an intrinsic feature but greatly vary depending on the habitat they inhabit. Compared to other habitats, groundwater fed sand filters impose strong purifying selection and low recombination. Together, this study improves understanding of interactions and evolution of species in the wild, and sheds light on the environmental dependency of evolutionary processes.

Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps

“…Based on the pN/pS values (0-1.43, 0.16 on average), these genes were under strong purifying selection. The evolutionary fitness of these three key functional genes was also consistent with that observed in previous studies for natural comammox Nitrospira populations 44 and Thalassospira bacterial populations isolated from million-year-old subseafloor sediments 19 . Our findings are in line with research showing that essential genes and enzymes catalyzing reactions that are difficult to bypass through alternative pathways are subject to higher purifying selection than nonessential ones 26, 44 .…”

“…The evolutionary fitness of these three key functional genes was also consistent with that observed in previous studies for natural comammox Nitrospira populations 44 and Thalassospira bacterial populations isolated from million-year-old subseafloor sediments 19 . Our findings are in line with research showing that essential genes and enzymes catalyzing reactions that are difficult to bypass through alternative pathways are subject to higher purifying selection than nonessential ones 26, 44 . Even though the pN/pS values of the vast majority were well below 1 (indicating purifying selection), genes with pN/pS values above 1 and significantly higher than the genomic average were detected, which indicates that positive selection acted upon those genes.…”

“…Population diversity in these groups as measured by SNVs/kbp is higher than that observed for soils in grassland meadows and subseafloor crustal fluids 17, 29 . These result indicate that deeply buried cold seep populations from MOB, ANME and SRB are under purifying selection, suggesting the possibility that these populations have reached an adaptive optimum for this stable environment, which is maintained by purging nonsynonymous mutations 44 . This result is in line with previous observations reported for bacterioplankton assemblages in sunlit freshwater and marine systems 16, 24, 45 , and microbial populations in other deep sea biospheres 46, 47 .…”

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

“…Multiple strains co‐occur within Microcoleus mats, but most mats are strongly dominated by a single strain. Nucleotide diversity was relatively low, up to ten times lower than values reported in soils (Crits‐Christoph et al, 2020 ), Nitrospira in drinking water filters (Palomo et al, 2020 ), and planktonic Microcystis blooms (Sabart et al, 2009 ; Tanabe et al, 2007 ). Microcoleus mats were thinner in smaller subwatersheds, probably due to light limitation and cooler temperatures, but these had similar nucleotide diversity to thicker mats collected from sunnier warmer sites with larger upstream subwatersheds (Figure 4b ).…”