Colony organization in the green alga Botryococcus braunii (Race B) is specified by a complex extracellular matrix

Taylor Weiss, Robyn Roth, Carrie Goodson, Stanislav Vitha, Ian Black, Parastoo Azadi, Jannette Rusch, Andreas Holzenburg, Timothy P. Devarenne, Ursula Goodenough

Research output: Contribution to journalArticle

87 Citations (Scopus)

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. 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.

Original languageEnglish (US)
Pages (from-to)1424-1440
Number of pages17
JournalEukaryotic Cell
Volume11
Issue number12
DOIs
StatePublished - Dec 1 2012
Externally publishedYes

Fingerprint

Chlorophyta
Hydrocarbons
Extracellular Matrix
Organizations
Endoplasmic Reticulum
Cell Wall
Cell Membrane
Arabinose
Extracellular Space
Golgi Apparatus
Chloroplasts
Nuclear Family
Galactose
Morphogenesis
Polysaccharides
Electron Microscopy
Mothers

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Colony organization in the green alga Botryococcus braunii (Race B) is specified by a complex extracellular matrix. / Weiss, Taylor; Roth, Robyn; Goodson, Carrie; Vitha, Stanislav; Black, Ian; Azadi, Parastoo; Rusch, Jannette; Holzenburg, Andreas; Devarenne, Timothy P.; Goodenough, Ursula.

In: Eukaryotic Cell, Vol. 11, No. 12, 01.12.2012, p. 1424-1440.

Research output: Contribution to journalArticle

Weiss, T, Roth, R, Goodson, C, Vitha, S, Black, I, Azadi, P, Rusch, J, Holzenburg, A, Devarenne, TP & Goodenough, U 2012, 'Colony organization in the green alga Botryococcus braunii (Race B) is specified by a complex extracellular matrix', Eukaryotic Cell, vol. 11, no. 12, pp. 1424-1440. https://doi.org/10.1128/EC.00184-12
Weiss, Taylor ; Roth, Robyn ; Goodson, Carrie ; Vitha, Stanislav ; Black, Ian ; Azadi, Parastoo ; Rusch, Jannette ; Holzenburg, Andreas ; Devarenne, Timothy P. ; Goodenough, Ursula. / Colony organization in the green alga Botryococcus braunii (Race B) is specified by a complex extracellular matrix. In: Eukaryotic Cell. 2012 ; Vol. 11, No. 12. pp. 1424-1440.
@article{caa29777e27648099e8992c7b56533a0,
title = "Colony organization in the green alga Botryococcus braunii (Race B) 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. 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.",
author = "Taylor Weiss and Robyn Roth and Carrie Goodson and Stanislav Vitha and Ian Black and Parastoo Azadi and Jannette Rusch and Andreas Holzenburg and Devarenne, {Timothy P.} and Ursula Goodenough",
year = "2012",
month = "12",
day = "1",
doi = "10.1128/EC.00184-12",
language = "English (US)",
volume = "11",
pages = "1424--1440",
journal = "Eukaryotic Cell",
issn = "1535-9778",
publisher = "American Society for Microbiology",
number = "12",

}

TY - JOUR

T1 - Colony organization in the green alga Botryococcus braunii (Race B) is specified by a complex extracellular matrix

AU - Weiss, Taylor

AU - Roth, Robyn

AU - Goodson, Carrie

AU - Vitha, Stanislav

AU - Black, Ian

AU - Azadi, Parastoo

AU - Rusch, Jannette

AU - Holzenburg, Andreas

AU - Devarenne, Timothy P.

AU - Goodenough, Ursula

PY - 2012/12/1

Y1 - 2012/12/1

N2 - 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. 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.

AB - 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. 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.

UR - http://www.scopus.com/inward/record.url?scp=84870407838&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84870407838&partnerID=8YFLogxK

U2 - 10.1128/EC.00184-12

DO - 10.1128/EC.00184-12

M3 - Article

VL - 11

SP - 1424

EP - 1440

JO - Eukaryotic Cell

JF - Eukaryotic Cell

SN - 1535-9778

IS - 12

ER -