"Why do viruses sense light?": A distinct abundant group of microbial rhodopsins discovered using functional metagenomics

Alina Pushkarev ¹ Keiichi Inoue ^2,4,5,9 Daniella Schatz ³ Ritsu Mizutori ² Yumeka Yamauchi ² Masae Konno ² Shirley Larom ¹ José Flores-Uribe ¹ Manish Singh ² Sahoko Tomida ² Shota Ito ² Ryoko Nakamura ² Satoshi P. Tsunoda ² Alon Philosof ¹ Itai Sharon ^6,7 Natalya Yutin ⁸ Eugene V. Koonin ⁸ Assaf Vardi ³ Hideki Kandori ^2,9 Oded Béjà ¹

¹Faculty of Biology, Technion – Israel Institute of Technology, Israel
²Department of Life Science and Applied Chemistry, Nagoya Institute of Technology, Japan
³Department of Plant and Environmental Sciences, Weizmann Institute of Science, Israel
⁴Frontier Research Institute for Material Science, Nagoya Institute of Technology, Japan
⁵Presto, Japan Science and Technology Agency, Japan
⁶Research Institute, Migal Galilee, Israel
⁷College, Tel Hai, Israel
⁸National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, USA
⁹Optobiotechnology Research Center, Nagoya Institute of Technology, Japan

Many organisms capture or sense sunlight using rhodopsin pigments, including type-1 microbial rhodopsins and type-2 animal rhodopsins. Here, using functional metagenomics, we report a previously unnoticed, diverse family, heliorhodopsins, which are distantly related to other rhodopsins and assume the opposite membrane topology compared to type-1 and type-2 rhodopsins, with the N-terminus facing the cell cytoplasm. Heliorhodopsins show photocycles >1 sec when expressed in Escherichia coli, suggestive of light sensory activity. Heliorhodopsins are abundant and distributed globally, being detected in soil, freshwater, marine and hypersaline environments, and in psychrophilic, mesophilic and even hyperthermophilic microbes including archaea, bacteria, eukarya and their viruses.

Emiliania huxleyi is a photosynthetic bloom-forming alga, causing gigantic blooms in the ocean. One of the main pathogens of these marine alga are specific large dsDNA viruses Emiliania huxleyi virus (EhV) that infect and can induce collapse of these blooms. It has been recently shown that light plays a major part in this infection cycle. The reason for the light dependent success of infection was pinned on the host and the energetic balance during photosynthesis.

Surprisingly, heliorhodopsin genes were found in the genomes of all known E. huxleyi viruses, but not in their host. The occurrence of light sensing protein in a virus involved in a light dependent infection brings new questions to this intriguing interaction. We speculate that the existence of a light sensing protein in the virus, may suggest that the virus itself is able to sense light and better prepare itself for infection.