Diversity, distribution, and expression of opsin genes in freshwater lakes

Abstract

Microbial opsin genes are widely distributed in aquatic environments and may significantly contribute to phototrophy and energy budgets in global oceans. However, the study of freshwater opsin genes has been largely limited. Here, we explored Type I opsin gene diversity, ecological distribution, and expression in lakes with contrasting physicochemical and optical characteristics. Using metagenomes and derived draft genomes from a clearwater lake and a humic bog, we recovered opsin genes from Actinobacteria, Proteobacteria, Bacteroidetes, Verrucomicrobia, Planctomycetes, Chloroflexi, and Candidatus Saccharibacteria. Most were predicted to encode green light-absorbing proton pumps within the proteorhodopsin and xanthorhodopsin groups, with the humic bog harboring much less diversity. Notably, viral opsin and novel actinobacterial opsin genes phylogenetically significantly different from the typical actinorhodopsin were recovered. Analyses of the surface layer of 33 freshwater systems revealed an inverse correlation between opsin gene abundance and lake dissolved organic carbon (DOC). In humic water with high terrestrial DOC and light-absorbing humic substances, opsin gene abundance was low and dramatically declined within the first few meters, whereas the abundance remained relatively high along the bulk water column in clearwater lakes with low DOC. These results suggest opsin gene distribution is influenced by lake optical properties and DOC. Gene expression analysis confirmed the significance of opsin-based phototrophy in clearwater lakes and revealed different diel expressional patterns among major phyla. Overall, our analyses recovered novel diversity, revealed distribution patterns, confirmed opsin gene expression, and suggested the significance of rhodopsin-based phototrophy in freshwater energy budgets, especially in clearwater lakes.