No heliorhodopsins in Gram-negative bacteria

Can this finding hint on the possible role of heliorhodopsins?
Published in Microbiology
No heliorhodopsins in Gram-negative bacteria

 Heliorhodopsins, a unique microbial rhodopsin family, were discovered only recently using functional metagenomics (see our behind the paper on heliorhodopsins). These rhodopsins exhibit very slow photocycles, possibly indicative of a light sensory function. In addition, their orientation in the membrane is opposite to that of other known rhodopsin types (microbial type-1 or animal type-2 rhodopsins). Heliorhodopsins are widespread and could be found in diverse bacteria, archaea, unicellular eukarya and even in algal viruses and originate from diverse habitats. 

Strangely, we observed that heliorhodopsins are completely missing in genomes from cultured Proteobacteria, a phylum in which diverse type-1 microbial rhodopsins are readily detected. As heliorhodopsins could be found in various uncultured microbial groups, we conducted a wide bioinformatic search on numerous environmental samples ranging from diverse habitats, to confirm our initial observation. 

Organic-rich sediment (“sapropel”) core from Lake Tekirghiol, Romania, collected by a sediment corer for microbial community analysis. Samples collected from multiple layers are used for DNA extraction (photo credit: Tiberiu Szöke-Nagy)

Overall, we analyzed about 138 million ORFs coming from a wide range of environments (including seawater, sediments, freshwater etc.), finding no heliorhodopsin genes affiliated with Proteobacteria. Surprisingly, none of the heliorhodopsin genes were affiliated with any other diderm group (Aquificae, Chlamydiae, Bacteroidetes, Chlorobi, Cyanobacteria, Fibrobacteres, Verrucomicrobia, Planctomycetes, Acidobacteria), except for 2 instances in Spirochetes (diderms are microbes possessing an outer-membrane in addition to their cytoplasmic membrane). 


Sampling of marine microbial and viral communities from surface water in the Red Sea. Water is pumped with peristaltic pumps and microorganisms are size fractionated by passing through filters of different sizes (photo credit: Shirley Larom)

One hypothesis is that heliorhodopsins have evolved solely in monoderms  (microbes possessing only a cytoplasmic membrane). Yet, we think such an explanation is less plausible, as lateral gene transfer is frequently observed with ‘regular’ type-1 rhodopsins, which can be found in both diderms and monoderms. Another hypothesis is related to the most apparent difference between the two groups, i.e. the presence and absence of an outer membrane in diderms and monoderms respectively. The outer membrane is an asymmetric bilayer composed of glycolipid lipopolysaccharides and glycerol phospholipids. It serves as a semi-permeable barrier and can block passage of different glycopeptides and amphiphilic compounds or even light if heavily pigmented. Therefore, we hypothesize that the lack of outer membrane in monoderms can suggest on the possible involvement of heliorhodopsins in light dependent transport of such compounds. 


Can you suggest different explanations for the absence of heliorhodopsins in diderms? Ideas are very welcome.

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