Potential Rhodopsin and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier

Abstract

Conserving additional energy from sunlight through bacteriochlorophyll (BChl)-based reaction center or proton-pumping rhodopsin is a highly successful life strategy in environmental bacteria. Rhodopsin and BChl based systems display contrasting characteristics in the size of coding operon, cost of biosynthesis, ease of expression control, and efficiency of energy production. This raises an intriguing question of whether a single bacterium has evolved the ability to perform these two types of phototrophy complementarily according to energy needs and environmental conditions. Here we report four Tardiphaga sp. strains (Alphaproteobacteria) of monophyletic origin isolated from a high Arctic glacier in northeast Greenland (81.566{degrees} N, 16.363{degrees} W) that are at different evolutionary stages concerning phototrophy. Their >99.8% identical genomes contain footprints of horizontal operon transfers (HOT) of the complete gene clusters encoding BChl and xanthorhodopsin (XR)-based dual phototrophy. Two strains only possess a complete xanthorhodopsin (XR) operon, while the other two strains have both a photosynthesis gene cluster (PGC) and an XR operon in their genomes. All XR operons are heavily surrounded by mobile genetic elements and located close to a tRNA gene, strongly signaling that a HOT event of XR operon has occurred recently. Mining public genome databases and our High Arctic glacial and soil metagenomes revealed that phylogenetically diverse bacteria have the metabolic potential of performing BChl and rhodopsin-based dual phototrophy. Our data provide new insights on how bacteria cope with the harsh and energy-deficient environments in surface glaciers, possibly by maximizing the capability of exploiting solar energy. ImportanceOver billions of years of evolution, bacteria capable of light-driven energy production have occupied every corner of surface Earth where solar irradiation can reach. Only two general biological systems have evolved in bacteria to be capable of net energy conservation via light-harvesting: one is based on the pigment of (bacterio-)chlorophyll and the other based on light-sensing retinal molecules. There is emerging genomic evidence that these two rather different systems can co-exist in a single bacterium to take advantage of their contrasting characteristics in the number of genes involved, biosynthesis cost, ease of expression control and efficiency of energy production, and thus enhance the capability of exploiting solar energy. Our data provide the first clear-cut evidence that such dual phototrophy potentially exist in glacial bacteria. Further public genome mining suggests this understudied dual phototrophic mechanism is possibly more common than our data alone suggested. Sequence data availabilityGenomes, metagenomes and raw reads were deposited into GenBank under Bioprojects PRJNA548505 and PRJNA552582.