Taxonomy and functional interactions in upper and bottom waters of an oligotrophic high-mountain deep lake (Redon, Pyrenees) unveiled by microbial metagenomics

Abstract

High mountain lakes are, in general, highly sensitive systems to external forcing and good sentinels of global environmental changes. For a better understanding of internal lake processes, we examined microbial biodiversity and potential biogeochemical interactions in the oligotrophic deep high-mountain Lake Redon (Pyrenees, 2240m altitude) using shotgun metagenomics. We analyzed the two ends of the range of environmental conditions found in Lake Redon, at 2 and 60 m depths. Bacteria were the most abundant component of the metagenomic reads (> 90%) and the diversity indices of both taxonomic (16S and 18S rRNA) and functional (carbon-, nitrogen-, sulfur-, and phosphorous-cycling) related genes were higher in the bottom dark layer than in the upper compartment. A marked segregation was observed both in biodiversity and in the dominant energy and biomass generating pathways between the extremes. The aerobic respiration was mainly dominated by heterotrophic Burkholderiales at the top and Actinobacteria and Burkholderiales at the lake bottom. The potential for an active nitrogen cycle (nitrogen fixation, nitrification, nitrite oxidation, and nitrate reduction) was mainly found at 60 m, and potential for methanogenesis, anaerobic ammonia oxidation and dissimilatory sulfur pathways were only observed there. Some unexpected and mostly unseen energy and biomass pathways were found relevant for the biogeochemical cycling in lake Redon, i.e., those related to carbon monoxide oxidation and phosphonates processing. We provide a general scheme of the main biogeochemical processes that may operate in the sentinel deep Lake Redon. This framework may help for a better understanding of the whole lake metabolism.