Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium " Chlorochromatium aggregatum"

Zhenfeng Liu, Johannes Müller, Tao Li, Richard M. Alvey, Kajetan Vogl, Niels Ulrik Frigaard, Nathan C. Rockwell, Eric S. Boyd, Lynn P. Tomsho, Stephan C. Schuster, Petra Henke, Manfred Rohde, Jörg Overmann, Donald Ashley Bryant

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Background: 'Chlorochromatium aggregatum' is a phototrophic consortium, a symbiosis that may represent the highest degree of mutual interdependence between two unrelated bacteria not associated with a eukaryotic host. 'Chlorochromatium aggregatum' is a motile, barrel-shaped aggregate formed from a single cell of 'Candidatus Symbiobacter mobilis" , a polarly flagellated, non-pigmented, heterotrophic bacterium, which is surrounded by approximately 15 epibiont cells of Chlorobium chlorochromatii, a non-motile photolithoautotrophic green sulfur bacterium.Results: We analyzed the complete genome sequences of both organisms to understand the basis for this symbiosis. Chl. chlorochromatii has acquired relatively few symbiosis-specific genes; most acquired genes are predicted to modify the cell wall or function in cell-cell adhesion. In striking contrast, 'Ca. S. mobilis' appears to have undergone massive gene loss, is probably no longer capable of independent growth, and thus may only reproduce when consortia divide. A detailed model for the energetic and metabolic bases of the dependency of 'Ca. S. mobilis' on Chl. chlorochromatii is described.Conclusions: Genomic analyses suggest that three types of interactions lead to a highly sophisticated relationship between these two organisms. Firstly, extensive metabolic exchange, involving carbon, nitrogen, and sulfur sources as well as vitamins, occurs from the epibiont to the central bacterium. Secondly, 'Ca. S. mobilis' can sense and move towards light and sulfide, resources that only directly benefit the epibiont. Thirdly, electron cycling mechanisms, particularly those mediated by quinones and potentially involving shared protonmotive force, could provide an important basis for energy exchange in this and other symbiotic relationships.

Original languageEnglish (US)
Article numberR127
JournalGenome biology
Volume14
Issue number11
DOIs
StatePublished - Nov 22 2013

Fingerprint

Symbiosis
epibiont
symbiosis
genomics
Bacteria
bacterium
bacteria
Chlorobium
Chlorobi
Genes
gene
Quinones
genes
organisms
sulfur
Sulfides
cells
cell aggregates
energy transfer
quinones

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Cell Biology

Cite this

Liu, Zhenfeng ; Müller, Johannes ; Li, Tao ; Alvey, Richard M. ; Vogl, Kajetan ; Frigaard, Niels Ulrik ; Rockwell, Nathan C. ; Boyd, Eric S. ; Tomsho, Lynn P. ; Schuster, Stephan C. ; Henke, Petra ; Rohde, Manfred ; Overmann, Jörg ; Bryant, Donald Ashley. / Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium " Chlorochromatium aggregatum". In: Genome biology. 2013 ; Vol. 14, No. 11.
@article{6f7bc3b9d828482b94e44f97c4261097,
title = "Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium {"} Chlorochromatium aggregatum{"}",
abstract = "Background: 'Chlorochromatium aggregatum' is a phototrophic consortium, a symbiosis that may represent the highest degree of mutual interdependence between two unrelated bacteria not associated with a eukaryotic host. 'Chlorochromatium aggregatum' is a motile, barrel-shaped aggregate formed from a single cell of 'Candidatus Symbiobacter mobilis{"} , a polarly flagellated, non-pigmented, heterotrophic bacterium, which is surrounded by approximately 15 epibiont cells of Chlorobium chlorochromatii, a non-motile photolithoautotrophic green sulfur bacterium.Results: We analyzed the complete genome sequences of both organisms to understand the basis for this symbiosis. Chl. chlorochromatii has acquired relatively few symbiosis-specific genes; most acquired genes are predicted to modify the cell wall or function in cell-cell adhesion. In striking contrast, 'Ca. S. mobilis' appears to have undergone massive gene loss, is probably no longer capable of independent growth, and thus may only reproduce when consortia divide. A detailed model for the energetic and metabolic bases of the dependency of 'Ca. S. mobilis' on Chl. chlorochromatii is described.Conclusions: Genomic analyses suggest that three types of interactions lead to a highly sophisticated relationship between these two organisms. Firstly, extensive metabolic exchange, involving carbon, nitrogen, and sulfur sources as well as vitamins, occurs from the epibiont to the central bacterium. Secondly, 'Ca. S. mobilis' can sense and move towards light and sulfide, resources that only directly benefit the epibiont. Thirdly, electron cycling mechanisms, particularly those mediated by quinones and potentially involving shared protonmotive force, could provide an important basis for energy exchange in this and other symbiotic relationships.",
author = "Zhenfeng Liu and Johannes M{\"u}ller and Tao Li and Alvey, {Richard M.} and Kajetan Vogl and Frigaard, {Niels Ulrik} and Rockwell, {Nathan C.} and Boyd, {Eric S.} and Tomsho, {Lynn P.} and Schuster, {Stephan C.} and Petra Henke and Manfred Rohde and J{\"o}rg Overmann and Bryant, {Donald Ashley}",
year = "2013",
month = "11",
day = "22",
doi = "10.1186/gb-2013-14-11-r127",
language = "English (US)",
volume = "14",
journal = "Genome Biology",
issn = "1474-7596",
publisher = "BioMed Central",
number = "11",

}

Liu, Z, Müller, J, Li, T, Alvey, RM, Vogl, K, Frigaard, NU, Rockwell, NC, Boyd, ES, Tomsho, LP, Schuster, SC, Henke, P, Rohde, M, Overmann, J & Bryant, DA 2013, 'Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium " Chlorochromatium aggregatum"', Genome biology, vol. 14, no. 11, R127. https://doi.org/10.1186/gb-2013-14-11-r127

Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium " Chlorochromatium aggregatum". / Liu, Zhenfeng; Müller, Johannes; Li, Tao; Alvey, Richard M.; Vogl, Kajetan; Frigaard, Niels Ulrik; Rockwell, Nathan C.; Boyd, Eric S.; Tomsho, Lynn P.; Schuster, Stephan C.; Henke, Petra; Rohde, Manfred; Overmann, Jörg; Bryant, Donald Ashley.

In: Genome biology, Vol. 14, No. 11, R127, 22.11.2013.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium " Chlorochromatium aggregatum"

AU - Liu, Zhenfeng

AU - Müller, Johannes

AU - Li, Tao

AU - Alvey, Richard M.

AU - Vogl, Kajetan

AU - Frigaard, Niels Ulrik

AU - Rockwell, Nathan C.

AU - Boyd, Eric S.

AU - Tomsho, Lynn P.

AU - Schuster, Stephan C.

AU - Henke, Petra

AU - Rohde, Manfred

AU - Overmann, Jörg

AU - Bryant, Donald Ashley

PY - 2013/11/22

Y1 - 2013/11/22

N2 - Background: 'Chlorochromatium aggregatum' is a phototrophic consortium, a symbiosis that may represent the highest degree of mutual interdependence between two unrelated bacteria not associated with a eukaryotic host. 'Chlorochromatium aggregatum' is a motile, barrel-shaped aggregate formed from a single cell of 'Candidatus Symbiobacter mobilis" , a polarly flagellated, non-pigmented, heterotrophic bacterium, which is surrounded by approximately 15 epibiont cells of Chlorobium chlorochromatii, a non-motile photolithoautotrophic green sulfur bacterium.Results: We analyzed the complete genome sequences of both organisms to understand the basis for this symbiosis. Chl. chlorochromatii has acquired relatively few symbiosis-specific genes; most acquired genes are predicted to modify the cell wall or function in cell-cell adhesion. In striking contrast, 'Ca. S. mobilis' appears to have undergone massive gene loss, is probably no longer capable of independent growth, and thus may only reproduce when consortia divide. A detailed model for the energetic and metabolic bases of the dependency of 'Ca. S. mobilis' on Chl. chlorochromatii is described.Conclusions: Genomic analyses suggest that three types of interactions lead to a highly sophisticated relationship between these two organisms. Firstly, extensive metabolic exchange, involving carbon, nitrogen, and sulfur sources as well as vitamins, occurs from the epibiont to the central bacterium. Secondly, 'Ca. S. mobilis' can sense and move towards light and sulfide, resources that only directly benefit the epibiont. Thirdly, electron cycling mechanisms, particularly those mediated by quinones and potentially involving shared protonmotive force, could provide an important basis for energy exchange in this and other symbiotic relationships.

AB - Background: 'Chlorochromatium aggregatum' is a phototrophic consortium, a symbiosis that may represent the highest degree of mutual interdependence between two unrelated bacteria not associated with a eukaryotic host. 'Chlorochromatium aggregatum' is a motile, barrel-shaped aggregate formed from a single cell of 'Candidatus Symbiobacter mobilis" , a polarly flagellated, non-pigmented, heterotrophic bacterium, which is surrounded by approximately 15 epibiont cells of Chlorobium chlorochromatii, a non-motile photolithoautotrophic green sulfur bacterium.Results: We analyzed the complete genome sequences of both organisms to understand the basis for this symbiosis. Chl. chlorochromatii has acquired relatively few symbiosis-specific genes; most acquired genes are predicted to modify the cell wall or function in cell-cell adhesion. In striking contrast, 'Ca. S. mobilis' appears to have undergone massive gene loss, is probably no longer capable of independent growth, and thus may only reproduce when consortia divide. A detailed model for the energetic and metabolic bases of the dependency of 'Ca. S. mobilis' on Chl. chlorochromatii is described.Conclusions: Genomic analyses suggest that three types of interactions lead to a highly sophisticated relationship between these two organisms. Firstly, extensive metabolic exchange, involving carbon, nitrogen, and sulfur sources as well as vitamins, occurs from the epibiont to the central bacterium. Secondly, 'Ca. S. mobilis' can sense and move towards light and sulfide, resources that only directly benefit the epibiont. Thirdly, electron cycling mechanisms, particularly those mediated by quinones and potentially involving shared protonmotive force, could provide an important basis for energy exchange in this and other symbiotic relationships.

UR - http://www.scopus.com/inward/record.url?scp=84887978108&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84887978108&partnerID=8YFLogxK

U2 - 10.1186/gb-2013-14-11-r127

DO - 10.1186/gb-2013-14-11-r127

M3 - Article

VL - 14

JO - Genome Biology

JF - Genome Biology

SN - 1474-7596

IS - 11

M1 - R127

ER -