Microbial rhodopsins are increasingly favoured over chlorophyll in High Nutrient Low Chlorophyll waters.

Microbial rhodopsins are simple light-harvesting complexes that, unlike chlorophyll photosystems, have no iron requirements for their synthesis and phototrophic functions. Here, we report the environmental concentrations of rhodopsin along the Subtropical Frontal Zone off New Zealand, where Subtropical waters encounter the iron-limited Subantarctic High Nutrient Low Chlorophyll (HNLC) region. Rhodopsin concentrations were highest in HNLC waters where chlorophyll-a concentrations were lowest. Furthermore, while the ratio of rhodopsin to chlorophyll-a photosystems was on average 20 along the transect, this ratio increased to over 60 in HNLC waters. We further show that microbial rhodopsins are abundant in both picoplankton (0.2-3 μm) and in the larger (>3 μm) size fractions of the microbial community containing eukaryotic plankton and/or particle-attached prokaryotes. These findings suggest that rhodopsin phototrophy could be critical for microbial plankton to adapt to resource-limiting environments where photosynthesis and possibly cellular respiration are impaired.

[1]  J. Fuhrman,et al.  Microbial rhodopsins are major contributors to the solar energy captured in the sea , 2019, Science Advances.

[2]  J. Fuhrman,et al.  Proteorhodopsins dominate the expression of phototrophic mechanisms in seasonal and dynamic marine picoplankton communities , 2018, PeerJ.

[3]  J. Raven,et al.  Living off the Sun: chlorophylls, bacteriochlorophylls and rhodopsins , 2018, Photosynthetica.

[4]  K. Johnson,et al.  The integral role of iron in ocean biogeochemistry , 2017, Nature.

[5]  J. E. Hallsworth,et al.  Metagenomic analysis reveals unusually high incidence of proteorhodopsin genes in the ultraoligotrophic Eastern Mediterranean Sea , 2017, Environmental microbiology.

[6]  Tihana Mirkovic,et al.  Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms. , 2017, Chemical reviews.

[7]  S. Sander,et al.  Spatial and seasonal variations of iron speciation in surface waters of the Subantarctic front and the Otago Continental Shelf , 2015 .

[8]  K. Currie,et al.  Bacterioplankton carbon cycling along the Subtropical Frontal Zone off New Zealand , 2015 .

[9]  A. Marchetti,et al.  Marine diatom proteorhodopsins and their potential role in coping with low iron availability , 2015, The ISME Journal.

[10]  D. Kirchman,et al.  Bioenergetics of photoheterotrophic bacteria in the oceans. , 2013, Environmental microbiology reports.

[11]  Omri M. Finkel,et al.  Global abundance of microbial rhodopsins , 2012, The ISME Journal.

[12]  P. Ralph,et al.  Diel variation of chlorophyll-a fluorescence, phytoplankton pigments and productivity in the Sub-Antarctic and Polar Front Zones south of Tasmania, Australia , 2011 .

[13]  Daniel Patrick Smith,et al.  Energy Starved Candidatus Pelagibacter Ubique Substitutes Light-Mediated ATP Production for Endogenous Carbon Respiration , 2011, PloS one.

[14]  R. Neutze,et al.  Proteorhodopsin Phototrophy Promotes Survival of Marine Bacteria during Starvation , 2010, PLoS biology.

[15]  M. Cottrell,et al.  Abundant proteorhodopsin genes in the North Atlantic Ocean. , 2007, Environmental microbiology.

[16]  R. Neutze,et al.  Light stimulates growth of proteorhodopsin-containing marine Flavobacteria , 2007, Nature.

[17]  E. Koonin,et al.  Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. , 2000, Science.

[18]  B. Tilbrook,et al.  The annual fCO2 cycle and the air–sea CO2 flux in the sub‐Antarctic Ocean , 1999 .

[19]  W. Sunda,et al.  Interrelated influence of iron, light and cell size on marine phytoplankton growth , 1997, Nature.

[20]  P. Tortell,et al.  The role of heterotrophic bacteria in iron-limited ocean ecosystems , 1996, Nature.

[21]  J. Raven The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources , 1988 .

[22]  J. Jillett Seasonal hydrology of waters off the Otago peninsula, South‐Eastern New Zealand , 1969 .

[23]  M. Kane,et al.  Quantification of endogenous retinoids. , 2010, Methods in molecular biology.

[24]  J. P. Dunne,et al.  High-latitude controls of thermocline nutrients and low latitude biological productivity , 2004, Nature.