Light-driven increase in carbon yield is linked to maintenance in the proteorhodopsin-containing Photobacterium angustum S14

Abstract

A type of photoheterotrophic bacteria contain a transmembrane light-driven proton pump called proteorhodopsins (PRs). Due to the prevalence of these organisms in the upper water column of the World’s Ocean, and their potential for light-driven ATP generation, they have been suggested to significantly influence energy and matter flows in the biosphere. To date, evidence for the significance of the light-driven metabolism of PR-containing prokaryotes has been obtained by comparing growth in batch culture, under light versus dark conditions, and it appears that responses to light are linked to unfavorable conditions, which so far have not been well parameterized. We studied light responses to carbon yields of the PR-containing Photobacterium angustum S14 using continuous culture conditions and light–dark cycles. We observed significant effects of light–dark cycles compared to dark controls, as well as significant differences between samples after 12 h illumination versus 12 h darkness. However, these effects were only observed under higher cell counts and lower pH associated with higher substrate concentrations. Under these substrate levels Pirt’s maintenance coefficient was higher when compared to lower substrate dark controls, and decreased under light–dark cycles. It appears that light responses by P. angustum S14 are induced by the energetic status of the cells rather than by low substrate concentrations.

Substrate-Limited and -Unlimited Coastal Microbial Communities Show Different Metabolic Responses with Regard to Temperature

“…Even the average value of Y = 0.34 of the chemostats (Figure 3 ) is higher than most oceanographic reports (López-Urrutia and Morán, 2007 ), but similar to mesocosm results (Dinasquet et al, 2013 ). In glucose-limited chemostat cultures (25°C, dilution rate 2.4 day −1 ) of a proteorhodopsin containing marine bacterium Courties et al ( 2015 ) reported an average Y of 0.57; using Equation (2) we calculated their specific respiration rate to be 1.8 day −1 which would place their result close to our regression in Figure 1 . We suggest that our high Y values are due to different aspects of our methodological approach: the use of glucose as an easily metabolized substrate; and the calculation of Y based on the measurement of respired CO 2 and POC to define microbial biomass.…”

The interplay between iron limitation, light and carbon in the proteorhodopsin-containing Photobacterium angustum S14

“…AND4 where an enhanced survival upon starvation conditions occurred by means of a series of dilution experiments (Gómez-Consarnau et al 2010;Akram et al 2013). The effect of light on P. angustum S14 in the context of maintenance energy and carbon yield had previously been studied using continuous culture experiments (Courties et al 2015). When correcting for variations in the dilution rates, Courties et al (2015) reported an increase in the carbon yield for cells subjected to light and dark cycles compared to dark controls.…”

“…The effect of light on P. angustum S14 in the context of maintenance energy and carbon yield had previously been studied using continuous culture experiments (Courties et al 2015). When correcting for variations in the dilution rates, Courties et al (2015) reported an increase in the carbon yield for cells subjected to light and dark cycles compared to dark controls. It was predicted that higher carbon yields resulted from a lower maintenance coefficient that could be attributed to PR activity although PR gene expression had not been measured in these experiments.…”

Distribution and Diversity of Rhodopsin-Producing Microbes in the Chesapeake Bay

“…If microbial rhodopsins are critical to the starvation response, they should only be expressed when cells are carbon or energy limited. Upregulation of proton-pumping rhodopsin expression under carbon-or energy-limited conditions has been observed in some bacterial isolates (3)(4)(5)(6)(20)(21)(22)(23). However, other work has identified bacterial species with rhodopsins that pump ions other than protons (24,25) and proton-pumping rhodopsins that energize active transport rather than ATP synthesis (26), as well as species whose rhodopsin expression is associated with anaplerotic CO 2 assimilation in the light (27)(28)(29).…”