Abstract
Proteorhodopsin is a light-activated retinal-containing proton pump found in many marine bacteria. These photoproteins are globally distributed in the ocean’s photic zone and are capable of generating a proton motive force across the cell membrane. We investigated the phylogenetic diversity, distribution, and abundance of proteorhodopsin encoding genes in free-living bacterioplankton in the North Pacific Subtropical Gyre, leveraging a gene catalog derived from metagenomic samples from the ocean’s surface to 1000 m depth. Proteorhodopsin genes were identified at all depths sampled, but were most abundant at depths shallower than 200 m. The majority of proteorhodopsin gene sequences (60.9%) belonged to members of the SAR11 lineage, with remaining sequences distributed among other diverse taxa. We observed variations in the conserved residues involved in ion pumping and spectral tuning, and biochemically confirmed four different proton pumping proteorhodopsin motifs, including one unique to deep-water SAR11. We also identified a new group of putative proteorhodopsins having unknown function. Our results reveal a broad organismal and unexpected depth distribution for different proteorhodopsin types, as well as substantial within-taxon variability. These data provide a framework for exploring the ecological relevance of proteorhodopsins and their spatiotemporal variation and function in heterotrophic bacteria in the open ocean.
Highlights
Two principal molecular mechanisms are known to exist in bacteria and archaea for harvesting light energy: chlorophyll-based photosystems and microbial (Type I) rhodopsins [1, 2]
To further characterize rhodopsin distribution and variability in the marine environment, we investigated the phylogenetic diversity, distribution, and abundance of proteorhodopsin groups derived from an extensive catalog of genes assembled from metagenomic depth profiles of freeliving bacterioplankton at Station ALOHA in the North Pacific Subtropical Gyre (NPSG) [38]
A minimum estimate of 1510 unique proteorhodopsin genes were identified in a catalog of approximately 8.9 million non-redundant gene sequences (95% nucleotide ID) originating from Station ALOHA
Summary
Two principal molecular mechanisms are known to exist in bacteria and archaea for harvesting light energy: chlorophyll-based photosystems and microbial (Type I) rhodopsins [1, 2]. Rhodopsins are retinal-based photoreceptors found in the genomes of bacteria inhabiting both freshwater and marine environments. They are known to be present in members of all three cellular domains of life. [3,4,5,6] and viruses [7, 8] These photoreceptor proteins have evolved to perform several different biological functions including ion transport, light sensing, and gene regulation [9,10,11]. Most marine bacterial proteorhodopsins characterized so far appear to be proton pumps, are expressed in native marine microbial populations, and are capable of functioning in energy production [5, 15, 16,17,18,19]. Light appears to be commonly utilized as a supplemental energy source in heterotrophic bacterial carbon and energy cycling in the sea
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