Genomic Makeup of the Marine Flavobacterium Nonlabens (Donghaeana) dokdonensis and Identification of a Novel Class of Rhodopsins

Abstract

Rhodopsin-containing marine microbes such as those in the class Flavobacteriia play a pivotal role in the biogeochemical cycle of the euphotic zone (Fuhrman JA, Schwalbach MS, Stingl U. 2008. Proteorhodopsins: an array of physiological roles? Nat Rev Microbiol. 6:488–494). Deciphering the genome information of flavobacteria and accessing the diversity and ecological impact of microbial rhodopsins are important in understanding and preserving the global ecosystems. The genome sequence of the orange-pigmented marine flavobacterium Nonlabens dokdonensis (basonym: Donghaeana dokdonensis) DSW-6 was determined. As a marine photoheterotroph, DSW-6 has written in its genome physiological features that allow survival in the oligotrophic environments. The sequence analysis also uncovered a gene encoding an unexpected type of microbial rhodopsin containing a unique motif in addition to a proteorhodopsin gene and a number of photolyase or cryptochrome genes. Homologs of the novel rhodopsin gene were found in other flavobacteria, alphaproteobacteria, a species of Cytophagia, a deinococcus, and even a eukaryote diatom. They all contain the characteristic NQ motif and form a phylogenetically distinct group. Expression analysis of this rhodopsin gene in DSW-6 indicated that it is induced at high NaCl concentrations, as well as in the presence of light and the absence of nutrients. Genomic and metagenomic surveys demonstrate the diversity of the NQ rhodopsins in nature and the prevalent occurrence of the encoding genes among microbial communities inhabiting hypersaline niches, suggesting its involvement in sodium metabolism and the sodium-adapted lifestyle.

Using Total Internal Reflection Fluorescence Microscopy To Visualize Rhodopsin-Containing Cells

“…In nonmarine aquatic environments, 35 to 62% of genomes within metagenomic assemblies harbor a rhodopsin (14), while analysis of freshwater bacterioplankton metagenomic assemblies and single amplified genomes from the same locations suggested the presence of a rhodopsin in 37 to 56% and 8 to 20% of the samples, respectively (35). These studies have demonstrated that rhodopsins are both more abundant and more diverse than previously suspected (10,(36)(37)(38). However, metagenomic and metatranscriptomic data cannot demonstrate that a rhodopsin is functional, nor can they consistently identify the organism that hosts the rhodopsin.…”

A light-driven sodium ion pump in marine bacteria

“…In contrast, a light-driven proton pump KR1 grows slowly, suggesting different functional roles other than generation of membrane potential. After submission of this paper, one paper was reported in which the presence of a light-driven sodium ion pump was proposed based on an enhanced expression of a marine bacterium at high salt concentration 45 . The present results are fully consistent with their proposal, and a light-driven sodium ion pump is now experimentally proven.…”

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

“…2), one containing rhodopsins pumping sodium and another containing rhodopsins pumping chloride. The sodium pumps have been found in Bacteroidetes, as well as in members of the Deinococcus-Thermus phylum isolated from very different environments (40,87,88). Interestingly, sodium pumps have been shown to have dual functionality, transporting protons and halogens depending on the chemical environment (40,50,89).…”