Widespread use of proton-pumping rhodopsin in Antarctic phytoplankton

Abstract

Photosynthetic carbon (C) fixation by phytoplankton in the Southern Ocean (SO) plays a critical role in regulating air–sea exchange of carbon dioxide and thus global climate. In the SO, photosynthesis (PS) is often constrained by low iron, low temperatures, and low but highly variable light intensities. Recently, proton-pumping rhodopsins (PPRs) were identified in marine phytoplankton, providing an alternate iron-free, light-driven source of cellular energy. These proteins pump protons across cellular membranes through light absorption by the chromophore retinal, and the resulting pH energy gradient can then be used for active membrane transport or for synthesis of adenosine triphosphate. Here, we show that PPR is pervasive in Antarctic phytoplankton, especially in iron-limited regions. In a model SO diatom, we found that it was localized to the vacuolar membrane, making the vacuole a putative alternative phototrophic organelle for light-driven production of cellular energy. Unlike photosynthetic C fixation, which decreases substantially at colder temperatures, the proton transport activity of PPR was unaffected by decreasing temperature. Cellular PPR levels in cultured SO diatoms increased with decreasing iron concentrations and energy production from PPR photochemistry could substantially augment that of PS, especially under high light intensities, where PS is often photoinhibited. PPR gene expression and high retinal concentrations in phytoplankton in SO waters support its widespread use in polar environments. PPRs are an important adaptation of SO phytoplankton to growth and survival in their cold, iron-limited, and variable light environment.

Variability in the phytoplankton response to upwelling across an iron limitation mosaic within the California current system

“…These results are consistent with previous studies that have also observed increased ISIPs and RHO expression in diatoms to cope with Fe stress (Cohen et al 2017; Behnke and LaRoche 2020). The significantly increased expression of RHO with respect to the DFB treatment could suggest the potential usage of an Fe‐independent energy production/conservation strategy by diatoms under Fe limiting conditions (Marchetti et al 2015; Andrew et al 2023; Strauss et al 2023). Although DFB is not necessarily a quantitative predictor of future Fe limitation, it does present a scenario of how declining Fe bioavailability can influence diatom physiology and gene expression.…”

Temporal dynamics and biogeography of sympagic and planktonic autotrophic microbial eukaryotes during the under-ice Arctic bloom

“…Gains and losses of species in response to the ongoing changes in Arctic habitats (e.g., decrease in sea ice coverage and increased seawater temperature) are likely to induce significant food web reorganization with potential cascade effects (Beaugrand et al 2019; Kortsch et al 2015). Microbial eukaryotes differ in their thermal tolerance (Demory et al 2019), dispersal capacity (Villarino et al 2018) and ability to exploit new resources, (Andrew et al 2023) which contributes to their abundance and diversity patterns. Therefore, they are natural proxies of community turnover and ecosystem shifts.…”

Proton-pumping rhodopsins promote the growth and survival of phytoplankton in a highly variable ocean

“…These membrane proteins contain the embedded pigment retinal, and upon absorption of light, the pigment–protein complex transports a hydrogen ion across the cellular membrane in which the PPR is embedded. The resultant membrane pH gradient can then be used to drive active membrane transport of essential nutrients and biomolecules and to synthesize adenosine triphosphate (ATP), the energy currency of the cell [ 7 , 8 ].…”

“…Recent experiments with the marine diatom Pseudo-nitzschia subcurvata isolated from the cold, iron-poor waters of the Southern Ocean (SO) have shown that PPR is localized in the vacuolar membrane of this species [ 7 ]. Experiments with this and two other SO diatoms ( Chaetoceros sociales and Synedra hyperborea ) showed that cellular PPR levels increased in low-iron cultures [ 7 ].…”

“…Recent experiments with the marine diatom Pseudo-nitzschia subcurvata isolated from the cold, iron-poor waters of the Southern Ocean (SO) have shown that PPR is localized in the vacuolar membrane of this species [ 7 ]. Experiments with this and two other SO diatoms ( Chaetoceros sociales and Synedra hyperborea ) showed that cellular PPR levels increased in low-iron cultures [ 7 ]. Energetic calculations with the three PPRs containing SO diatoms suggest that light-driven cellular energy production by PPR could substantially augment or exceed that from photosynthesis under certain environmental conditions, namely, high light intensity, cold temperatures, and low availability of the micronutrient iron [ 7 ].…”