The structural and functional role of carotenoids in chlorosomes

Chlorosomes are large light-harvesting complexes found in three phyla of anoxygenic photosynthetic bacteria. Chlorosomes are primarily composed of self-assembling pigment aggregates. In addition to the main pigment, bacteriochlorophyll c, d, or e, chlorosomes also contain variable amounts of carotenoids. Here, we use X-ray scattering and electron cryomicroscopy, complemented with absorption spectroscopy and pigment analysis, to compare the morphologies, structures, and pigment compositions of chlorosomes from Chloroflexus aurantiacus grown under two different light conditions and Chlorobaculum tepidum. High-purity chlorosomes from C. aurantiacus contain about 20% more carotenoid per bacteriochlorophyll c molecule when grown under low light than when grown under high light. This accentuates the light-harvesting function of carotenoids, in addition to their photoprotective role. The low-light chlorosomes are thicker due to the overall greater content of pigments and contain domains of lamellar aggregates. Experiments where carotenoids were selectively extracted from intact chlorosomes using hexane proved that they are located in the interlamellar space, as observed previously for species belonging to the phylum Chlorobi. A fraction of the carotenoids are localized in the baseplate, where they are bound differently and cannot be removed by hexane. In C. tepidum, carotenoids cannot be extracted by hexane even from the chlorosome interior. The chemical structure of the pigments in C. tepidum may lead to π-π interactions between carotenoids and bacteriochlorophylls, preventing carotenoid extraction. The results provide information about the nature of interactions between bacteriochlorophylls and carotenoids in the protein-free environment of the chlorosome interior.

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Main Authors: Psencik, Jakub, Arellano, Juan B., Collins, Aaron M., Laurinmäki, Pasi A., Torkkeli, Mika, Löflund, Benita, Serimaa, Ritva E., Blankenship, Robert E., Butcher, Sarah J.
Format: artículo biblioteca
Language:English
Published: American Society for Microbiology 2013-04
Subjects:Chlorosomes, Carotenoids, Bacteriochlorophylls, Llamellar aggregates, X-ray scattering, pi-pi interactions,
Online Access:http://hdl.handle.net/10261/90198
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spelling dig-irnasa-es-10261-901982021-12-27T15:59:56Z The structural and functional role of carotenoids in chlorosomes Psencik, Jakub Arellano, Juan B. Collins, Aaron M. Laurinmäki, Pasi A. Torkkeli, Mika Löflund, Benita Serimaa, Ritva E. Blankenship, Robert E. Butcher, Sarah J. Chlorosomes Carotenoids Bacteriochlorophylls Llamellar aggregates X-ray scattering pi-pi interactions Chlorosomes are large light-harvesting complexes found in three phyla of anoxygenic photosynthetic bacteria. Chlorosomes are primarily composed of self-assembling pigment aggregates. In addition to the main pigment, bacteriochlorophyll c, d, or e, chlorosomes also contain variable amounts of carotenoids. Here, we use X-ray scattering and electron cryomicroscopy, complemented with absorption spectroscopy and pigment analysis, to compare the morphologies, structures, and pigment compositions of chlorosomes from Chloroflexus aurantiacus grown under two different light conditions and Chlorobaculum tepidum. High-purity chlorosomes from C. aurantiacus contain about 20% more carotenoid per bacteriochlorophyll c molecule when grown under low light than when grown under high light. This accentuates the light-harvesting function of carotenoids, in addition to their photoprotective role. The low-light chlorosomes are thicker due to the overall greater content of pigments and contain domains of lamellar aggregates. Experiments where carotenoids were selectively extracted from intact chlorosomes using hexane proved that they are located in the interlamellar space, as observed previously for species belonging to the phylum Chlorobi. A fraction of the carotenoids are localized in the baseplate, where they are bound differently and cannot be removed by hexane. In C. tepidum, carotenoids cannot be extracted by hexane even from the chlorosome interior. The chemical structure of the pigments in C. tepidum may lead to π-π interactions between carotenoids and bacteriochlorophylls, preventing carotenoid extraction. The results provide information about the nature of interactions between bacteriochlorophylls and carotenoids in the protein-free environment of the chlorosome interior. This study was supported by grants from the Academy of Finland (1213467 and 1129684 Centre of Excellence in Virus Research 2006-2011 to S.J.B. and R.T.; 1118462 to R.T), Biocentrum Helsinki (S.J.B.), and the Czech Science Foundation (project P501/12/G055 to J.P.). C. aurantiacus cell growth and sample preparation was carried out by A.M.C. as part of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under award number DE-SC 0001035. Peer reviewed 2014-01-30T13:09:23Z 2014-01-30T13:09:23Z 2013-04 artículo http://purl.org/coar/resource_type/c_6501 Journal of Bacteriology 195(8): 1727-1734 (2013) http://hdl.handle.net/10261/90198 10.1128/JB.02052-12 23396908 en http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3624547/pdf/zjb1727.pdf open American Society for Microbiology
institution IRNASA ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-irnasa-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IRNASA España
language English
topic Chlorosomes
Carotenoids
Bacteriochlorophylls
Llamellar aggregates
X-ray scattering
pi-pi interactions
Chlorosomes
Carotenoids
Bacteriochlorophylls
Llamellar aggregates
X-ray scattering
pi-pi interactions
spellingShingle Chlorosomes
Carotenoids
Bacteriochlorophylls
Llamellar aggregates
X-ray scattering
pi-pi interactions
Chlorosomes
Carotenoids
Bacteriochlorophylls
Llamellar aggregates
X-ray scattering
pi-pi interactions
Psencik, Jakub
Arellano, Juan B.
Collins, Aaron M.
Laurinmäki, Pasi A.
Torkkeli, Mika
Löflund, Benita
Serimaa, Ritva E.
Blankenship, Robert E.
Butcher, Sarah J.
The structural and functional role of carotenoids in chlorosomes
description Chlorosomes are large light-harvesting complexes found in three phyla of anoxygenic photosynthetic bacteria. Chlorosomes are primarily composed of self-assembling pigment aggregates. In addition to the main pigment, bacteriochlorophyll c, d, or e, chlorosomes also contain variable amounts of carotenoids. Here, we use X-ray scattering and electron cryomicroscopy, complemented with absorption spectroscopy and pigment analysis, to compare the morphologies, structures, and pigment compositions of chlorosomes from Chloroflexus aurantiacus grown under two different light conditions and Chlorobaculum tepidum. High-purity chlorosomes from C. aurantiacus contain about 20% more carotenoid per bacteriochlorophyll c molecule when grown under low light than when grown under high light. This accentuates the light-harvesting function of carotenoids, in addition to their photoprotective role. The low-light chlorosomes are thicker due to the overall greater content of pigments and contain domains of lamellar aggregates. Experiments where carotenoids were selectively extracted from intact chlorosomes using hexane proved that they are located in the interlamellar space, as observed previously for species belonging to the phylum Chlorobi. A fraction of the carotenoids are localized in the baseplate, where they are bound differently and cannot be removed by hexane. In C. tepidum, carotenoids cannot be extracted by hexane even from the chlorosome interior. The chemical structure of the pigments in C. tepidum may lead to π-π interactions between carotenoids and bacteriochlorophylls, preventing carotenoid extraction. The results provide information about the nature of interactions between bacteriochlorophylls and carotenoids in the protein-free environment of the chlorosome interior.
format artículo
topic_facet Chlorosomes
Carotenoids
Bacteriochlorophylls
Llamellar aggregates
X-ray scattering
pi-pi interactions
author Psencik, Jakub
Arellano, Juan B.
Collins, Aaron M.
Laurinmäki, Pasi A.
Torkkeli, Mika
Löflund, Benita
Serimaa, Ritva E.
Blankenship, Robert E.
Butcher, Sarah J.
author_facet Psencik, Jakub
Arellano, Juan B.
Collins, Aaron M.
Laurinmäki, Pasi A.
Torkkeli, Mika
Löflund, Benita
Serimaa, Ritva E.
Blankenship, Robert E.
Butcher, Sarah J.
author_sort Psencik, Jakub
title The structural and functional role of carotenoids in chlorosomes
title_short The structural and functional role of carotenoids in chlorosomes
title_full The structural and functional role of carotenoids in chlorosomes
title_fullStr The structural and functional role of carotenoids in chlorosomes
title_full_unstemmed The structural and functional role of carotenoids in chlorosomes
title_sort structural and functional role of carotenoids in chlorosomes
publisher American Society for Microbiology
publishDate 2013-04
url http://hdl.handle.net/10261/90198
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