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Title: Specific Glucoside Transporters Influence Septal Structure and Function in the Filamentous, Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120

Abstract

When deprived of combined nitrogen, some filamentous cyanobacteria contain two cell types: vegetative cells that fix CO2 through oxygenic photosynthesis and heterocysts that are specialized in N2 fixation. In the diazotrophic filament, the vegetative cells provide the heterocysts with reduced carbon (mainly in the form of sucrose) and heterocysts provide the vegetative cells with combined nitrogen. Septal junctions traverse peptidoglycan through structures known as nanopores and appear to mediate intercellular molecular transfer that can be traced with fluorescent markers, including the sucrose analog esculin (a coumarin glucoside) that is incorporated into the cells. Uptake of esculin by the model heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 was inhibited by the α-glucosides sucrose and maltose. Analysis of Anabaena mutants identified components of three glucoside transporters that move esculin into the cells: GlsC (Alr4781) and GlsP (All0261) are an ATP-binding subunit and a permease subunit of two different ABC transporters, respectively, and HepP (All1711) is a major facilitator superfamily (MFS) protein that was shown previously to be involved in formation of the heterocyst envelope. Transfer of fluorescent markers (especially calcein) between vegetative cells of Anabaena was impaired by mutation of glucoside transporter genes. GlsP and HepP interact in bacterial two-hybrid assays withmore » the septal junction-related protein SepJ, and GlsC was found to be necessary for the formation of a normal number of septal peptidoglycan nanopores and for normal subcellular localization of SepJ. Therefore, beyond their possible role in nutrient uptake in Anabaena, glucoside transporters influence the structure and function of septal junctions. Heterocyst-forming cyanobacteria have the ability to perform oxygenic photosynthesis and to assimilate atmospheric CO2 and N2. These organisms grow as filaments that fix these gases specifically in vegetative cells and heterocysts, respectively. For the filaments to grow, these types of cells exchange nutrients, including sucrose, which serves as a source of reducing power and of carbon skeletons for the heterocysts. Movement of sucrose between cells in the filament takes place through septal junctions and has been traced with a fluorescent sucrose analog, esculin, that can be taken up by the cells. Here, we identified α-glucoside transporters of Anabaena« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [3];  [4];  [2]; ORCiD logo [1]
  1. Consejo Superior de Investigaciones Científicas (CSIC) and Univ. de Sevilla, Seville (Spain). Inst. de Bioquímica Vegetal y Fotosíntesis
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.
  3. Imperial College, London (United Kingdom). Dept. of Life Sciences
  4. Queen Mary Univ. of London, London (United Kingdom). School of Biological and Chemical Sciences
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); Plan Nacional de Investigación, Spain; European Regional Development
OSTI Identifier:
1474071
Grant/Contract Number:  
FG02-91ER20021; BFU2014-56757-P
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Volume: 199; Journal Issue: 7; Journal ID: ISSN 0021-9193
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Nieves-Morión, Mercedes, Lechno-Yossef, Sigal, López-Igual, Rocío, Frías, José E., Mariscal, Vicente, Nürnberg, Dennis J., Mullineaux, Conrad W., Wolk, C. Peter, and Flores, Enrique. Specific Glucoside Transporters Influence Septal Structure and Function in the Filamentous, Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120. United States: N. p., 2017. Web. doi:10.1128/JB.00876-16.
Nieves-Morión, Mercedes, Lechno-Yossef, Sigal, López-Igual, Rocío, Frías, José E., Mariscal, Vicente, Nürnberg, Dennis J., Mullineaux, Conrad W., Wolk, C. Peter, & Flores, Enrique. Specific Glucoside Transporters Influence Septal Structure and Function in the Filamentous, Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120. United States. https://doi.org/10.1128/JB.00876-16
Nieves-Morión, Mercedes, Lechno-Yossef, Sigal, López-Igual, Rocío, Frías, José E., Mariscal, Vicente, Nürnberg, Dennis J., Mullineaux, Conrad W., Wolk, C. Peter, and Flores, Enrique. Tue . "Specific Glucoside Transporters Influence Septal Structure and Function in the Filamentous, Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120". United States. https://doi.org/10.1128/JB.00876-16. https://www.osti.gov/servlets/purl/1474071.
@article{osti_1474071,
title = {Specific Glucoside Transporters Influence Septal Structure and Function in the Filamentous, Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120},
author = {Nieves-Morión, Mercedes and Lechno-Yossef, Sigal and López-Igual, Rocío and Frías, José E. and Mariscal, Vicente and Nürnberg, Dennis J. and Mullineaux, Conrad W. and Wolk, C. Peter and Flores, Enrique},
abstractNote = {When deprived of combined nitrogen, some filamentous cyanobacteria contain two cell types: vegetative cells that fix CO2 through oxygenic photosynthesis and heterocysts that are specialized in N2 fixation. In the diazotrophic filament, the vegetative cells provide the heterocysts with reduced carbon (mainly in the form of sucrose) and heterocysts provide the vegetative cells with combined nitrogen. Septal junctions traverse peptidoglycan through structures known as nanopores and appear to mediate intercellular molecular transfer that can be traced with fluorescent markers, including the sucrose analog esculin (a coumarin glucoside) that is incorporated into the cells. Uptake of esculin by the model heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 was inhibited by the α-glucosides sucrose and maltose. Analysis of Anabaena mutants identified components of three glucoside transporters that move esculin into the cells: GlsC (Alr4781) and GlsP (All0261) are an ATP-binding subunit and a permease subunit of two different ABC transporters, respectively, and HepP (All1711) is a major facilitator superfamily (MFS) protein that was shown previously to be involved in formation of the heterocyst envelope. Transfer of fluorescent markers (especially calcein) between vegetative cells of Anabaena was impaired by mutation of glucoside transporter genes. GlsP and HepP interact in bacterial two-hybrid assays with the septal junction-related protein SepJ, and GlsC was found to be necessary for the formation of a normal number of septal peptidoglycan nanopores and for normal subcellular localization of SepJ. Therefore, beyond their possible role in nutrient uptake in Anabaena, glucoside transporters influence the structure and function of septal junctions. Heterocyst-forming cyanobacteria have the ability to perform oxygenic photosynthesis and to assimilate atmospheric CO2 and N2. These organisms grow as filaments that fix these gases specifically in vegetative cells and heterocysts, respectively. For the filaments to grow, these types of cells exchange nutrients, including sucrose, which serves as a source of reducing power and of carbon skeletons for the heterocysts. Movement of sucrose between cells in the filament takes place through septal junctions and has been traced with a fluorescent sucrose analog, esculin, that can be taken up by the cells. Here, we identified α-glucoside transporters of Anabaena},
doi = {10.1128/JB.00876-16},
journal = {Journal of Bacteriology},
number = 7,
volume = 199,
place = {United States},
year = {Tue Jan 17 00:00:00 EST 2017},
month = {Tue Jan 17 00:00:00 EST 2017}
}

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The small Ca 2+ -binding protein CSE links Ca 2+ signalling with nitrogen metabolism and filament integrity in Anabaena sp. PCC 7120
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