Rhodopsin-Containing Microorganisms Thrive in High Nutrient Low Chlorophyll (HNLC) Sub-Antarctic Waters

Microbial rhodopsins are simple light-driven ion-pumps which unlike chlorophyll-a (chl-a) photosystems, have low nutrient (e.g., iron) requirements for their synthesis and phototrophic functions. Consistent with this notion, recent data has suggested that microbial rhodopsins might be particularly relevant in oligotrophic areas of the ocean such as the Eastern Mediterranean Sea. However, the effect of iron limitation on rhodopsins has only been studied in one strain of Pseudo-Nitszchia, showing rhodopsin synthesis upregulation under iron limitation. To date, rhodopsin distributions in natural microbial communities that inhabit high nutrient low chlorophyll (HNLC) regions have never been examined. Here, we report the first environmental concentrations of microbial rhodopsins along the Subtropical Frontal Zone off New Zealand, along the Munida Microbial Observatory Time-Series transect, which traverses the coastal neritic, subtropical, sub-Antarctic HNLC water masses, and their transition zones. As expected, the lowest chlorophyll values within the sampling transect were observed in the HNLC sub-Antarctic waters (100-140 pM), as compared to the coastal neritic (270-390 pM) or the subtropical waters (150-2800 pM) where iron is not limiting. However, rhodopsin concentrations appeared to be opposite to chlorophyll, reaching their highest concentrations (30 pM) at the stations where chl-a concentrations were the lowest in the HNLC. This trend was observed in both picoplankton (0.2-3µm) and plankton > 3 µm. Furthermore, the ratios of rhodopsin to chl-a appeared to be associated with water mass origin. For instance, rhodopsin/chl-a ratios ranged from 0.01 to 0.06 in the subtropical waters, increasing by > 3-fold in the HNLC waters. These findings support the idea that rhodopsins may help cope with iron-limiting conditions in natural microbial plankton where photosynthesis and possibly cellular respiration are impaired.