Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin

Abstract

Background Permanently stratified lakes contain diverse microbial communities that vary with depth and so serve as useful models for studying the relationships between microbial community structure and geochemistry. Recent work has shown that these lakes can also harbor numerous bacteria and archaea from novel lineages, including those from the Candidate Phyla Radiation (CPR). However, the extent to which geochemical stratification differentially impacts carbon metabolism and overall genetic potential in CPR bacteria compared to other organisms is not well defined. Results Here, we determine the distribution of microbial lineages along an oxygen gradient in Lac Pavin, a deep, stratified lake in central France, and examine the influence of this gradient on their metabolism. Genome-based analyses revealed an enrichment of distinct C1 and CO2 fixation pathways in the oxic lake interface and anoxic zone/sediments, suggesting that oxygen likely plays a role in structuring metabolic strategies in non-CPR bacteria and archaea. Notably, we find that the oxidation of methane and its byproducts is largely spatially separated from methane production, which is mediated by diverse communities of sediment methanogens that vary on the centimeter scale. In contrast, we detected evidence for RuBisCO throughout the water column and sediments, including form II/III and form III-related enzymes encoded by CPR bacteria in the water column and DPANN archaea in the sediments. On the whole, though, CPR bacteria and phages did not show strong signals of gene content differentiation by depth, despite the fact that distinct species groups populate different lake and sediment compartments. Conclusions Overall, our analyses suggest that environmental gradients in Lac Pavin select for capacities of CPR bacteria and phages to a lesser extent than for other bacteria and archaea. This may be due to the fact that selection in the former groups is indirect and depends primarily on host characteristics.

Stratified microbial communities in Australia’s only anchialine cave are taxonomically novel and drive chemotrophic energy production via coupled nitrogen-sulphur cycling

“…The relative abundance of genes that drive the reverse TCA cycle and Wood-Ljungdahl pathway increased with depth, which are the hypoxic regions of this system (Supplementary Table 1). Similar trends have been observed in hypoxic and anoxic zones of stratified water columns [62,63].…”

“…Methanol and formaldehyde oxidation (C1 metabolism), decreased with depth, while the methane monooxygenase gene, mmoB, involved in the first step of methane metabolism, increased with depth. Similar patterns of carbon metabolism genes have been observed over an oxygen gradient in a permanently stratified lake [63]. Arsenic and selenium cycling genes also corresponded to a depth gradient (Fig.…”

A pan‐genomic approach reveals novel Sulfurimonas clade in the ferruginous meromictic Lake Pavin

“…Bin58 and SAG 733‐F2 had ANIb and AAI of 99.8% and 98.7% respectively, and >99% with MAG LacPavin_0419_WC90 (Jaffe et al., 2023). The corresponding numbers for Bin76 fall below 84%, while it shares >97% with MAG LacPavin_0818_WC45 (Jaffe et al., 2023) (Figure 1).…”

“…Bin58 and SAG 733‐F2 had ANIb and AAI of 99.8% and 98.7% respectively, and >99% with MAG LacPavin_0419_WC90 (Jaffe et al., 2023). The corresponding numbers for Bin76 fall below 84%, while it shares >97% with MAG LacPavin_0818_WC45 (Jaffe et al., 2023) (Figure 1). These results confirm that Lake Pavin hosts two distinct Sulfurimonas species (threshold used for species demarcation >95% (Kim et al., 2014; Thompson et al., 2013)).…”

Macroevolutionary dynamics in micro-organisms: generalists give rise to specialists across biomes in the ubiquitous bacterial phylumMyxococcota

“…Although their capacity for dispersal means that adaptive radiations in prokaryotes are unlikely to arise via colonisation events of novel ecosystems, it may be that the uptake of novel traits through horizontal gene transfer (HGT) allows the colonisation of new niche space, which subsequently can be partitioned into different specialists. Going forward, combining targeted amplicon sequencing data with (metagenome-assisted) whole-genome data [2,6] is needed to characterise the role of HGT in evolutionary transitions and its mechanistic impact on ecological specialisation [2].…”