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. BChl and rhodopsin-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° N, 16.363° W) that are at different evolutionary stages concerning phototrophy. Their >99.8% identical genomes contain footprints of horizontal operon transfer (HOT) of the complete gene clusters encoding BChl- and xanthorhodopsin (XR)-based dual phototrophy. Two strains possess only a complete XR operon, while the other two strains have both a photosynthesis gene cluster and an XR operon in their genomes. All XR operons are heavily surrounded by mobile genetic elements and are located close to a tRNA gene, strongly signaling that a HOT event of the 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 environment in surface glacier, possibly by maximizing the capability of exploiting solar energy. IMPORTANCE Over the course of evolution for billions of years, bacteria that are capable of light-driven energy production have occupied every corner of surface Earth where sunlight 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 is based on proton-pumping rhodopsin. There is emerging genomic evidence that these two rather different systems can coexist 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 exists in glacial bacteria. Further public genome mining suggests this understudied dual phototrophic mechanism is possibly more common than our data alone suggested.

Gemmatimonas groenlandica sp. nov. Is an Aerobic Anoxygenic Phototroph in the Phylum Gemmatimonadetes

“…We applied these criteria and examined the six Gemmatimonadetes MAGs previously assembled from 460G-base shotgun reads of a surface soil sample (with prefix ES-bin) and a glacial ice sample (with prefix LF-bin) near the Villum Research Station (81°36′ N, 16°40′ W) in Northeast Greenland ( Zeng et al, 2020 ). Three bins (ES-bin-14, ES-bin-51, and LF-bin-339) were found to contain at least one puf gene, one puh gene, and one bch gene ( Table 3 ), indicating they belong to CGB.…”

“…The 16S rRNA gene reference sequences were downloaded from the NCBI nr database through BLASTn search (>97% identities, >1,375 bp, equivalent to >90% coverage). The reference sequences for acsF include the sequences downloaded from the NCBI nr database through tBLASTn search (>250 amino acids, equivalent to >70% coverage) and those used in two previous studies ( Zeng et al, 2016 , 2020 ). For phylogeny inference, sequences were first aligned with MAFFT v7.471 ( Katoh and Standley, 2013 ) using the Q-INS-i algorithm for 16S rRNA genes, which takes secondary structure information of RNA into account and the G-INS-I algorithm for AcsF protein sequences.…”

“…We previously reported six MAGs of Gemmatimonadetes origin in a metagenomics study of high arctic soil and glacier in Northeast Greenland ( Zeng et al, 2020 ). Detailed analysis of these MAGs other than general description was not carried out in that study.…”

“…Here we further present the functional genes and phylogenetic data of these Gemmatimonadetes MAGs with the aim to assess potential importance and metabolic diversity of phototrophic Gemmatimonadetes bacteria in Greenlandic environments. The six MAGs include ES-bin-14, ES-bin-29, ES-bin-51, and ES-bin-78 that were assembled from the exposed surface soil metagenome (designated ES) at the “Lille Firn” glacier (designated LF, GPS: 81.566° N, 16.363° W) close to the Villum Research Station in Northeast Greenland and the two bins LF-bin-215 and LF-bin-339 that were assembled from the LF surface ice metagenome (see more details on sampling in Zeng et al, 2020 ). The genome annotations of the MAGs were downloaded from the NCBI microbial genome portal via FTP.…”

Diversity of Aerobic Anoxygenic Phototrophs and Rhodopsin-Containing Bacteria in the Surface Microlayer, Water Column and Epilithic Biofilms of Lake Baikal

“…Planctomycetes seem to be associated primarily with particles, surfaces, microbial mats, and biofilms while they can be very abundant in other habitats as well [ 90 ]. The closest pufM homologue of Baikal representatives (MBC7770036, 98% similarity) was detected in a high arctic glacier in Northeast Greenland [ 91 ]. pufM -containing Planctomycetes were also reported in the South China Sea [ 92 ].…”