Simultaneous presence of bacteriochlorophyll and xanthorhodopsin genes in a freshwater bacterium

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DOI

  • Karel Kopejtka, Czech Academy of Sciences
  • ,
  • Jürgen Tomasch, Technical University of Braunschweig
  • ,
  • Yonghui Zeng, Czech Academy of Sciences
  • ,
  • Vadim Selyanin, Czech Academy of Sciences
  • ,
  • Marko Dachev, Czech Academy of Sciences
  • ,
  • Kasia Piwosz, Czech Academy of Sciences
  • ,
  • Martin Tichý, Czech Academy of Sciences
  • ,
  • David Bína, Czech Academy of Sciences, University of South Bohemia
  • ,
  • Zdenko Gardian, Czech Academy of Sciences, University of South Bohemia
  • ,
  • Boyke Bunk, German Collection of Microorganisms and Cell Cultures
  • ,
  • Henner Brinkmann, German Collection of Microorganisms and Cell Cultures
  • ,
  • Robert Geffers, Helmholtz Centre for Infection Research
  • ,
  • Ruben Sommaruga, University of Innsbruck
  • ,
  • Michal Koblížek, Czech Academy of Sciences

Photoheterotrophic bacteria represent an important part of aquatic microbial communities. There exist two fundamentally different light-harvesting systems: bacteriochlorophyll-containing reaction centers or rhodopsins. Here, we report a photoheterotrophic Sphingomonas strain isolated from an oligotrophic lake, which contains complete sets of genes for both rhodopsin-based and bacteriochlorophyllbased phototrophy. Interestingly, the identified genes were not expressed when cultured in liquid organic media. Using reverse transcription quantitative PCR (RT-qPCR), RNA sequencing, and bacteriochlorophyll a quantification, we document that bacteriochlorophyll synthesis was repressed by high concentrations of glucose or galactose in the medium. Coactivation of photosynthesis genes together with genes for TonBdependent transporters suggests the utilization of light energy for nutrient import. The photosynthetic units were formed by ring-shaped light-harvesting complex 1 and reaction centers with bacteriochlorophyll a and spirilloxanthin as the main lightharvesting pigments. The identified rhodopsin gene belonged to the xanthorhodopsin family, but it lacks salinixanthin antenna. In contrast to bacteriochlorophyll, the expression of xanthorhodopsin remained minimal under all experimental conditions tested. Since the gene was found in the same operon as a histidine kinase, we propose that it might serve as a light sensor. Our results document that photoheterotrophic Sphingomonas bacteria use the energy of light under carbon-limited conditions, while under carbon-replete conditions, they cover all their metabolic needs through oxidative phosphorylation. IMPORTANCE Phototrophic organisms are key components of many natural environments. There exist two main phototrophic groups: species that collect light energy using various kinds of (bacterio)chlorophylls and species that utilize rhodopsins. Here, we present a freshwater bacterium Sphingomonas sp. strain AAP5 which contains genes for both light-harvesting systems. We show that bacteriochlorophyll-based reaction centers are repressed by light and/or glucose. On the other hand, the rhodopsin gene was not expressed significantly under any of the experimental conditions. This may indicate that rhodopsin in Sphingomonas may have other functions not linked to bioenergetics.

OriginalsprogEngelsk
Artikelnummere01044-20
TidsskriftmSystems
Vol/bind5
Nummer6
DOI
StatusUdgivet - dec. 2020

Bibliografisk note

Funding Information:
This research was funded by the Czech Science Foundation project 18-14095Y awarded to K.P. M.K. and J.T. were funded by bilateral CSF DAAD project 57155424, and Z.G. thanks European Regional Development Fund-Project CZ.02.1.01/0.0/0.0/15_003/ 0000441. D.B. was supported by CSF project 19-28323X and RVO:60077344.

Publisher Copyright:
Copyright © 2020 Kopejtka et al.

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

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