Aquatic bacterial rhodopsin proton pumps harvest light energy for photoheterotrophic growth and are known to contain hydroxylated carotenoids that expand the wavelengths of light utilized, but these have not been characterized in marine archaea. Here, by combining a marine chromophore extract with purified archaeal rhodopsins identified in marine metagenomes, we show light energy transfer from diverse hydroxylated carotenoids to heimdallarchaeial rhodopsins (HeimdallRs) from uncultured marine planktonic members of 'Candidatus Kariarchaeaceae' ('Candidatus Asgardarchaeota'). These light-harvesting antennas absorb in the blue-light range and transfer energy to the green-light-absorbing retinal chromophore within HeimdallRs, enabling the use of light that is otherwise unavailable to the rhodopsin. Furthermore, we show elevated proton pumping by the antennas in HeimdallRs under white-light illumination, which better simulates the light conditions encountered by these archaea in their natural habitats. Our results indicate that light-harvesting antennas in microbial rhodopsins exist in families beyond xanthorhodopsins and proteorhodopsins and are present in both marine bacteria and archaea.
- MeSH
- Archaea * metabolismus genetika chemie MeSH
- archeální proteiny * metabolismus chemie genetika MeSH
- fylogeneze MeSH
- karotenoidy metabolismus chemie MeSH
- metagenom MeSH
- mořská voda mikrobiologie MeSH
- přenos energie MeSH
- rhodopsiny mikrobiální * chemie metabolismus MeSH
- rodopsin * chemie metabolismus MeSH
- světlo MeSH
- světlosběrné proteinové komplexy * chemie metabolismus MeSH
- vodní organismy metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- archeální proteiny * MeSH
- karotenoidy MeSH
- rhodopsiny mikrobiální * MeSH
- rodopsin * MeSH
- světlosběrné proteinové komplexy * MeSH
Recent advances in phylogenomic analyses and increased genomic sampling of uncultured prokaryotic lineages have brought compelling evidence in support of the emergence of eukaryotes from within the archaeal domain of life (eocyte hypothesis)1,2. The discovery of Asgardarchaeota and its supposed position at the base of the eukaryotic tree of life3,4 provided cues about the long-awaited identity of the eocytic lineage from which the nucleated cells (Eukaryota) emerged. While it is apparent that Asgardarchaeota encode a plethora of eukaryotic-specific proteins (the highest number identified yet in prokaryotes)5, the lack of genomic information and metabolic characterization has precluded inferences about their lifestyles and the metabolic landscape that favoured the emergence of the protoeukaryote ancestor. Here, we use advanced phylogenetic analyses for inferring the deep ancestry of eukaryotes, and genome-scale metabolic reconstructions for shedding light on the metabolic milieu of Asgardarchaeota. In doing so, we: (1) show that Heimdallarchaeia (the closest eocytic lineage to eukaryotes to date) are likely to have a microoxic niche, based on their genomic potential, with aerobic metabolic pathways that are unique among Archaea (that is, the kynurenine pathway); (2) provide evidence of mixotrophy within Asgardarchaeota; and (3) describe a previously unknown family of rhodopsins encoded within the recovered genomes.
- MeSH
- aerobióza MeSH
- anaerobióza MeSH
- Archaea klasifikace genetika metabolismus MeSH
- ekosystém MeSH
- fylogeneze * MeSH
- genom archeí genetika MeSH
- metabolické sítě a dráhy MeSH
- molekulární evoluce MeSH
- rhodopsiny mikrobiální klasifikace genetika MeSH
- RNA ribozomální genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- rhodopsiny mikrobiální MeSH
- RNA ribozomální MeSH