Extended temperature optimum of photosynthetic reaction centers in Rhodobacterales

Abstract

Temperature is one of the most important physical factors affecting microbial and biochemical processes. We investigated the performance of photosynthetic apparatus of marine photoheterotrophic bacterium Dinoroseobacter shibae under various temperatures. The primary photochemistry and electron transport was measured using variable infra-red fluorometry in the cells grown between 8-35°C. It was found that the photosynthetic electron transport had a broad temperature optimum between 25-50°C. Moreover, the primary charge separation stayed functional even after rising temperature up to 55°C. The same phenomenon was observed also in other phototrophic Rhodobacterales. The psychrotolerant bacterium Roseisalinus antarcticus reached its maximum electron transport rate at 48°C, 30°C above its growth temperature. We propose that the extended temperature stability may be crucial to maintain photosynthetic function under situation when photosynthetic membranes heat up above their ambient temperature due to the heat dissipation of the excess light energy.

Temperature dependence of photosynthetic reaction centre activity in Rhodospirillum rubrum

“…It is interesting to note that this maximum is 8 °C above the R. rubrum optimum growth temperature which is 33 °C (Kaiser and Oelze 1980a, b). A similar observation was made already before in the case of phototrophic bacterium Dinoroseobacter shibae from Rhodobacterales (Kaftan et al 2019) and mitochondria (Chrétien et al 2018). It was speculated that the elevated optimum of the electron-transfer activity may be connected with the necessity to cope with the heat dissipated during the photochemical reactions (Kaftan et al 2019).…”

“…Phylogenetically, it belongs to Rhodospirillales that is one of the main orders of Alphaproteobacteria. Also, Rhodospirillales represent the closest branch to Rhodobacterales, the subject of our previous study (Kaftan et al 2019). The temperature dependence of photosynthetic activity of R. rubrum was measured in vivo using bacteriochlorophyll (BChl) fluorometry and absorption spectroscopy providing information about primary photochemistry as well as electron-transport activity.…”

“…On the other hand, higher temperatures can facilitate electron transfer, but if too high, this may alter normal functioning of the photosynthetic reactions, resulting in the disruption and damage of the photosynthetic machinery (Odahara et al 2011). In our previous study with mesophilic phototrophic Rhodobacterales (class Alphaproteobacteria), we have shown that their reaction centres (RCs) have an optimum of electron transport between 40 and 50 °C (Kaftan et al 2019). The same optimum was also found for respiration in Dinoroseobacter shibae (Kaftan et al 2019).…”

“…In our previous study with mesophilic phototrophic Rhodobacterales (class Alphaproteobacteria), we have shown that their reaction centres (RCs) have an optimum of electron transport between 40 and 50 °C (Kaftan et al 2019). The same optimum was also found for respiration in Dinoroseobacter shibae (Kaftan et al 2019). This was significantly higher than the growth temperature of the respective organisms.…”

“…The same electron-transport optimum was also observed in Erythrobacter sp. NAP1 (Kaftan et al 2019). Erythrobacter belongs to the order Sphingomonadales within the Alphaproteobacteria, which indicates that the extended temperature optimum of the photosynthetic reactions may be a more general phenomenon.…”