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Title: Colony organization in the green alga Botryococcus braunii is specified by a complex extracellular matrix

Abstract

Botryococcus braunii is a colonial green alga whose cells associate via a complex extracellular matrix (ECM) and produce prodigious amounts of liquid hydrocarbons that can be readily converted into conventional combustion engine fuels. We used quickfreeze deep-etch electron microscopy and biochemical/histochemical analysis to elucidate many new features of B. braunii cell/colony organization and composition. Intracellular lipid bodies associate with the chloroplast and endoplasmic reticulum (ER) but show no evidence of being secreted. The ER displays striking fenestrations and forms a continuous subcortical system in direct contact with the cell membrane. The ECM has three distinct components. (i) Each cell is surrounded by a fibrous β-1, 4- and/or β-1, 3-glucan-containing cell wall. (ii) The intracolonial ECM space is filled with a cross-linked hydrocarbon network permeated with liquid hydrocarbons. (iii) Colonies are enclosed in a retaining wall festooned with a fibrillar sheath dominated by arabinose-galactose polysaccharides, which sequesters ECM liquid hydrocarbons. Each cell apex associates with the retaining wall and contributes to its synthesis. Retaining-wall domains also form "drapes" between cells, with some folding in on themselves and penetrating the hydrocarbon interior of a mother colony, partitioning it into daughter colonies. In addition, we propose that retaining-wall components are synthesized in themore » apical Golgi apparatus, delivered to apical ER fenestrations, and assembled on the surfaces of apical cell walls, where a proteinaceous granular layer apparently participates in fibril morphogenesis. We further propose that hydrocarbons are produced by the nonapical ER, directly delivered to the contiguous cell membrane, and pass across the nonapical cell wall into the hydrocarbon-based ECM.« less

Authors:
 [1];  [2];  [3];  [1];  [4];  [4];  [3];  [1];  [1];  [3]
  1. Texas A&M Univ., College Station, TX (United States)
  2. Washington Univ. School of Medicine, St. Louis, MO (United States)
  3. Washington Univ., St. Louis, MO (United States)
  4. Univ. of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
Texas A&M AgriLife Research, College Station, TX (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE)
OSTI Identifier:
1093826
Report Number(s):
DOE-DANF-0003046-P1
Journal ID: ISSN 1535-9778; 28302-P
Grant/Contract Number:  
EE0003046
Resource Type:
Accepted Manuscript
Journal Name:
Eukaryotic Cell
Additional Journal Information:
Journal Volume: 11; Journal Issue: 12; Journal ID: ISSN 1535-9778
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS

Citation Formats

Weiss, Taylor L., Roth, Robyn, Goodson, Carrie, Vithda, Stanislav, Black, Ian, Azadi, Parastoo, Rusch, Jannette, Holzenburg, Andreas, Devarenne, Timothy P., and Goodenough, Ursula. Colony organization in the green alga Botryococcus braunii is specified by a complex extracellular matrix. United States: N. p., 2012. Web. doi:10.1128/EC.00184-12.
Weiss, Taylor L., Roth, Robyn, Goodson, Carrie, Vithda, Stanislav, Black, Ian, Azadi, Parastoo, Rusch, Jannette, Holzenburg, Andreas, Devarenne, Timothy P., & Goodenough, Ursula. Colony organization in the green alga Botryococcus braunii is specified by a complex extracellular matrix. United States. https://doi.org/10.1128/EC.00184-12
Weiss, Taylor L., Roth, Robyn, Goodson, Carrie, Vithda, Stanislav, Black, Ian, Azadi, Parastoo, Rusch, Jannette, Holzenburg, Andreas, Devarenne, Timothy P., and Goodenough, Ursula. Fri . "Colony organization in the green alga Botryococcus braunii is specified by a complex extracellular matrix". United States. https://doi.org/10.1128/EC.00184-12. https://www.osti.gov/servlets/purl/1093826.
@article{osti_1093826,
title = {Colony organization in the green alga Botryococcus braunii is specified by a complex extracellular matrix},
author = {Weiss, Taylor L. and Roth, Robyn and Goodson, Carrie and Vithda, Stanislav and Black, Ian and Azadi, Parastoo and Rusch, Jannette and Holzenburg, Andreas and Devarenne, Timothy P. and Goodenough, Ursula},
abstractNote = {Botryococcus braunii is a colonial green alga whose cells associate via a complex extracellular matrix (ECM) and produce prodigious amounts of liquid hydrocarbons that can be readily converted into conventional combustion engine fuels. We used quickfreeze deep-etch electron microscopy and biochemical/histochemical analysis to elucidate many new features of B. braunii cell/colony organization and composition. Intracellular lipid bodies associate with the chloroplast and endoplasmic reticulum (ER) but show no evidence of being secreted. The ER displays striking fenestrations and forms a continuous subcortical system in direct contact with the cell membrane. The ECM has three distinct components. (i) Each cell is surrounded by a fibrous β-1, 4- and/or β-1, 3-glucan-containing cell wall. (ii) The intracolonial ECM space is filled with a cross-linked hydrocarbon network permeated with liquid hydrocarbons. (iii) Colonies are enclosed in a retaining wall festooned with a fibrillar sheath dominated by arabinose-galactose polysaccharides, which sequesters ECM liquid hydrocarbons. Each cell apex associates with the retaining wall and contributes to its synthesis. Retaining-wall domains also form "drapes" between cells, with some folding in on themselves and penetrating the hydrocarbon interior of a mother colony, partitioning it into daughter colonies. In addition, we propose that retaining-wall components are synthesized in the apical Golgi apparatus, delivered to apical ER fenestrations, and assembled on the surfaces of apical cell walls, where a proteinaceous granular layer apparently participates in fibril morphogenesis. We further propose that hydrocarbons are produced by the nonapical ER, directly delivered to the contiguous cell membrane, and pass across the nonapical cell wall into the hydrocarbon-based ECM.},
doi = {10.1128/EC.00184-12},
journal = {Eukaryotic Cell},
number = 12,
volume = 11,
place = {United States},
year = {Fri Aug 31 00:00:00 EDT 2012},
month = {Fri Aug 31 00:00:00 EDT 2012}
}

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