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

Abstract

SUMMARYThe recognition of a new family of rhodopsins in marine planktonic bacteria, proton-pumping proteorhodopsin, expanded the known phylogenetic range, environmental distribution, and sequence diversity of retinylidene photoproteins. At the time of this discovery, microbial ion-pumping rhodopsins were known solely in haloarchaea inhabiting extreme hypersaline environments. Shortly thereafter, proteorhodopsins and other light-activated energy-generating rhodopsins were recognized to be widespread among marine bacteria. The ubiquity of marine rhodopsin photosystems now challenges prior understanding of the nature and contributions of “heterotrophic” bacteria to biogeochemical carbon cycling and energy fluxes. Subsequent investigations have focused on the biophysics and biochemistry of these novel microbial rhodopsins, their distribution across the tree of life, evolutionary trajectories, and functional expression in nature. Later discoveries included the identification of proteorhodopsin genes in all three domains of life, the spectral tuning of rhodopsin variants to wavelengths prevailing in the sea, variable light-activated ion-pumping specificities among bacterial rhodopsin variants, and the widespread lateral gene transfer of biosynthetic genes for bacterial rhodopsins and their associated photopigments. Heterologous expression experiments with marine rhodopsin genes (and associated retinal chromophore genes) provided early evidence that light energy harvested by rhodopsins could be harnessed to provide biochemical energy. Importantly, some studies with native marine bacteria show that rhodopsin-containing bacteria use light to enhance growth or promote survival during starvation. We infer from the distribution of rhodopsin genes in diverse genomic contexts that different marine bacteria probably use rhodopsins to support light-dependent fitness strategies somewhere between these two extremes.

Effects of grazing, phosphorus and light on the growth rates of major bacterioplankton taxa in the coastal NW Mediterranean

“…dark treatments to obtain clues on their effect on the growth of different bacterial taxa, including those that contain photoheterotrophic members (Figs and ). The presence of PR‐containing bacteria is expected since SAR11 and Bacteroidetes were abundant in all treatments and both taxa contain a large proportion of photoheterotrophic members (see review by Pinhassi et al ., ). The relevance of AAP bacteria has been estimated in the BBMO in our previous studies (Ferrera et al ., ; Hojerová et al ., ).…”

“…Considering that marine photoheterotrophic bacteria are more the rule than the exception in nature (DeLong and Béjà, ), PAR needs to be considered a relevant environmental factor controlling the dynamics of heterotrophic bacteria when building carbon flow models (Gasol et al ., ). Whereas SAR11 bacteria and some taxa within the Gammaproteobateria or the Bacteroidetes among others can use light through proteorhodopsins (PR) (Pinhassi et al ., ), aerobic anoxygenic photrotrophic (AAP) bacteria can do so using bacteriochlorophyll a reaction centres (Koblížek, ). Current knowledge on the growth of photoheterotrophs indicates that while the most abundant PR bacteria (the SAR11 clade) grow slower than other taxa (Kirchman, ), AAP bacteria grow faster than average marine bacteria (Koblížek et al ., ; Ferrera et al ., ).…”

Microdiversity shapes the traits, niche space, and biogeography of microbial taxa

“…However, even though the acquisition of proteorhodopsin may result in cladogenesis, it is debatable whether the presence of proteorhodopsin represents a truly fundamental change in central metabolism. Research to date has shown that proteorhodopsin only confers photoheterotrophy and access to additional ATP sources, not photoautotrophy, and does not always promote growth under low nutrient conditions (Pinhassi et al ., ). Second, differences in growth optima between two closely related sub‐taxa are nearly always small, ranging only a few degrees in terms of temperature (Yung et al ., ) or a few μmol in terms of light (Moore and Chisholm, ).…”

Voltage imaging with genetically encoded indicators

“…Many potential novel scaffolds remain to be tested. Of the many thousands of microbial rhodopsins identified via metagenomic sequence analysis [64], only a handful have been tested as putative voltage sensors. Mitochondria and chloroplasts have molecular machinery for transmembrane electron transfer.…”