dinoflagellates use light with other mechanisms than photosystems

A bacterial proteorhodopsin proton pump in marine eukaryotes (Slamovits et al 2011)

A decade ago, a new form of phototrophy based on proteorhodopsin, a novel type of bacterial rhodopsin, was discovered in marine bacterioplankton. Proteorhodopsin-mediated phototrophy is now known from a wide variety of bacteria and archaea living in diverse environments, and is thought to be spread by horizontal transfer. Evidence shows that it promotes growth and survival in poor conditions. This study shows that one lineage of eukaryotes, dinoflagellates, has acquired multiple types of rhodopsin including proton-pumping proteorhodopsins of the type used for generating energy from light.

Sequence data and phylogenetic analysis was performed. 18, 102 genes where sequenced, grouped and related to each other. The sequences for the marine dinoflagellate predator Oxyrrhis marina were most intriguing. The sequences for rhodopsin related to other bacteria but not eukaryotes, and therefore horizontal gene transfer must have taken place.

The possible functional properties of the dinoflagellate rhodopsin where discussed. An ancient origin in an early ancestor of the O. marina lineage was suggested. Other genes found are assigned to a sensory role rather than the rhodopsin. Certain residues are conserved with the codes for retinal in certain positions to strongly suggest that O. marina proteorhodopsin is a proton pump. It is also possible that proteorhodopsin replaces or supplements the V-ATPase activity, acidifying digestive vacuoles using light rather than ATP. An intriguing possibility is that proteorhodopsin works in conjunction with vacuolar-type H + -pyrophosphatase, generating PPi as an alternative source of energy. Consistent with the ecology of O. marina there are specific residues that tune the spectral absorbance to green light. The sub-cellular locations of rhodopsin in O.marina where found using an immunoflouresence technique. Indications of cytosolic compartmentalization where seen but there was no evidence of localization of proteorhodopsin to the plasma membrane, nuclear or mitochondrial. Regardless of what this function might be, it must be non-essential in the short term, as it is in prokaryotes, because O. marina can be grown in total darkness. The abundance and diversity of rhodopsins in dinoflagellates is unexpected, given the relatively restricted distribution previously known in eukaryotes, suggesting that rhodopsin perhaps has a variety of sensory or regulatory roles in this lineage.

O. marina presents an intriguing mix of feeding strategies that are the sum of a winding path of evolution: the consummate predator that has in the course of evolution shed photosynthesis, only to regain a new version of phototrophy through horizontal gene transfer, perhaps from bacteria on which its ancestors had fed.