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

Alicia Courties,Philippe Lebaron,Alain Rapaport,Thomas Riedel,Marcelino T Suzuki

doi:10.3389/fmicb.2015.00688

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.

Highlights

A type of photoheterotrophic bacteria contain a transmembrane light-driven proton pump called proteorhodopsins (PRs)
In order to evaluate the effect of light on growth of P. angustum S14 in batch and estimate growth parameters, batch experiments were run in photobioreactors with the same medium, substrate, agitation and aeration as those used in continuous culture experiments at “high” (i.e., 3 mM glucose) substrate levels
As previously shown for the other members of the family Vibrionaceae (Gomez-Consarnau et al, 2010; Wang et al, 2012; Akram et al, 2013), P. angustum S14 shows no responses to light under “normal” batch growth, and this is becoming the norm for these organisms, whereas the picture is more complicated for the Flavobacteriaceae even when the same genus is considered (Gomez-Consarnau et al, 2007; Riedel et al, 2013)

Summary

Introduction

A type of photoheterotrophic bacteria contain a transmembrane light-driven proton pump called proteorhodopsins (PRs). More significantly a number of studies mostly using real-time PCR or genomic data (as PRs are difficult to detect directly) has shown that PRcontaining prokaryotes might represent a large proportion of the total bacterioplankton of the upper water column (e.g., Rusch et al, 2007; Campbell et al, 2008; Riedel et al, 2010; Finkel et al, 2013) These high abundances, combined with the potential roles of PR-based ATP generation suggest that these organisms might have a significant impact on the ecology and biogeochemistry of marine systems. PR-based ATP generation has been hypothesized to have possible effects in growth rates (Gomez-Consarnau et al, 2007; Fuhrman et al, 2008), carbon metabolism (Fuhrman et al, 2008; Gonzalez et al, 2008), transport (Fuhrman et al, 2008), as well as starvation survival (Gomez-Consarnau et al, 2010; Steindler et al, 2011; Akram et al, 2013) among others

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