title: Stimulation of growth by proteorhodopsin phototrophy involves regulation of central metabolic pathways in marine planktonic bacteria.
abstract: Proteorhodopsin (PR) is present in half of surface ocean bacterioplankton, where its light-driven proton pumping provides energy to cells. Indeed, PR promotes growth or survival in different bacteria. However, the metabolic pathways mediating the light responses remain unknown. We analyzed growth of the PR-containing Dokdonia sp. MED134 (where light-stimulated growth had been found) in seawater with low concentrations of mixed [yeast extract and peptone (YEP)] or single (alanine, Ala) carbon compounds as models for rich and poor environments. We discovered changes in gene expression revealing a tightly regulated shift in central metabolic pathways between light and dark conditions. Bacteria showed relatively stronger light responses in Ala compared with YEP. Notably, carbon acquisition pathways shifted toward anaplerotic CO2 fixation in the light, contributing 31 ± 8% and 24 ± 6% of the carbon incorporated into biomass in Ala and YEP, respectively. Thus, MED134 was a facultative double mixotroph, i.e., photo- and chemotrophic for its energy source and using both bicarbonate and organic matter as carbon sources. Unexpectedly, relative expression of the glyoxylate shunt genes (isocitrate lyase and malate synthase) was >300-fold higher in the light--but only in Ala--contributing a more efficient use of carbon from organic compounds. We explored these findings in metagenomes and metatranscriptomes and observed similar prevalence of the glyoxylate shunt compared with PR genes and highest expression of the isocitrate lyase gene coinciding with highest solar irradiance. Thus, regulatory interactions between dissolved organic carbon quality and central metabolic pathways critically determine the fitness of surface ocean bacteria engaging in PR phototrophy.
authors.affiliation: Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, SE-39182 Kalmar, Sweden;
authors.forename: Joakim
authors.initials: J
authors.lastname: Palovaara
authors.affiliation: Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, SE-39182 Kalmar, Sweden;
authors.forename: Neelam
authors.initials: N
authors.lastname: Akram
authors.affiliation: Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, SE-39182 Kalmar, Sweden;
authors.forename: Federico
authors.initials: F
authors.lastname: Baltar
authors.affiliation: Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, SE-39182 Kalmar, Sweden;
authors.forename: Carina
authors.initials: C
authors.lastname: Bunse
authors.affiliation: Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, SE-39182 Kalmar, Sweden;
authors.forename: Jeremy
authors.initials: J
authors.lastname: Forsberg
authors.affiliation: Department of Marine Biology and Oceanography, Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas, ES-08003 Barcelona, Spain; and.
authors.forename: Carlos
authors.initials: C
authors.lastname: Pedrós-Alió
authors.affiliation: Department of Microbiology, University of La Laguna, ES-38206 La Laguna, Spain.
authors.forename: José M
authors.initials: JM
authors.lastname: González
authors.affiliation: Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, SE-39182 Kalmar, Sweden; jarone.pinhassi@Lnu.se.
authors.forename: Jarone
authors.initials: J
authors.lastname: Pinhassi
mesh_terms: D000222:Adaptation, Physiological / Q000502:physiology; D001639:Bicarbonates / Q000378:metabolism; D018533:Biomass; D002244:Carbon / Q000378:metabolism; D002245:Carbon Dioxide / Q000378:metabolism; D041965:Flavobacteriaceae / Q000235:genetics / Q000378:metabolism*; D015964:Gene Expression Regulation, Bacterial; D008027:Light; D008386:Marine Biology; D053858:Metabolic Networks and Pathways / Q000235:genetics; D052817:Phototrophic Processes / Q000502:physiology*; D010933:Plankton / Q000235:genetics / Q000378:metabolism*; D012243:Rhodopsin / Q000235:genetics / Q000378:metabolism*; D025604:Rhodopsins, Microbial; D012623:Seawater / Q000382:microbiology
chemical_list: D001639:Bicarbonates; D025604:Rhodopsins, Microbial; C413548:proteorhodopsin; D002245:Carbon Dioxide; D002244:Carbon; D012243:Rhodopsin
keywords: gene expression regulation; microbial ecology; quantitative PCR