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Title: A paralog of a bacteriochlorophyll biosynthesis enzyme catalyzes the formation of 1,2-dihydrocarotenoids in green sulfur bacteria

Abstract

Chlorobaculum tepidum, a green sulfur bacterium, utilizes chlorobactene as its major carotenoid, and this organism also accumulates a reduced form of this monocyclic pigment, 1′,2′-dihydrochlorobactene. The protein catalyzing this reduction is the last unidentified enzyme in the biosynthetic pathways for all of the green sulfur bacterial pigments utilized for photosynthesis. The genome of C. tepidum contains two paralogous genes encoding members of the FixC family of flavoproteins: bchP, which has been shown to encode an enzyme of bacteriochlorophyll biosynthesis; and bchO, for which a function has not been assigned. Here we demonstrate that a bchO mutant is unable to synthesize 1′,2′-dihydrochlorobactene, and when bchO is heterologously expressed in a neurosporene-producing mutant of the purple bacterium, Rhodobacter sphaeroides, the encoded protein is able to catalyze the formation of 1,2-dihydroneurosporene, the major carotenoid of the only other organism reported to synthesize 1,2-dihydrocarotenoids, Blastochloris viridis. Identification of this enzyme completes the pathways for the synthesis of photosynthetic pigments in Chlorobiaceae, and accordingly and consistent with its role in carotenoid biosynthesis, we propose to rename the gene cruI. Importantly, the absence of cruI in B. viridis indicates that a second 1,2-carotenoid reductase, which is structurally unrelated to CruI (BchO), must exist in nature. Themore » evolution of this carotenoid reductase in green sulfur bacteria is discussed herein.« less

Authors:
 [1];  [2];  [2];  [3]; ORCiD logo [4]
  1. Univ. of Sheffield (United Kingdom); Pennsylvania State Univ., University Park, PA (United States)
  2. Pennsylvania State Univ., University Park, PA (United States)
  3. Univ. of Sheffield (United Kingdom)
  4. Pennsylvania State Univ., University Park, PA (United States); Montana State Univ., Bozeman, MT (United States)
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; European Research Council (ERC)
OSTI Identifier:
1547337
Grant/Contract Number:  
[FG02-94ER20137]
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
[ Journal Volume: 293; Journal Issue: 39]; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; photosynthesis; photosynthetic pigment; carotenoid; bacterial genetics; energy metabolism; Blastochloris viridis; Chlorobaculum tepidum; green sulfur bacterium; Rhodobacter sphaeroides

Citation Formats

Canniffe, Daniel P., Thweatt, Jennifer L., Gomez Maqueo Chew, Aline, Hunter, C. Neil, and Bryant, Donald A. A paralog of a bacteriochlorophyll biosynthesis enzyme catalyzes the formation of 1,2-dihydrocarotenoids in green sulfur bacteria. United States: N. p., 2018. Web. doi:10.1074/jbc.ra118.004672.
Canniffe, Daniel P., Thweatt, Jennifer L., Gomez Maqueo Chew, Aline, Hunter, C. Neil, & Bryant, Donald A. A paralog of a bacteriochlorophyll biosynthesis enzyme catalyzes the formation of 1,2-dihydrocarotenoids in green sulfur bacteria. United States. doi:10.1074/jbc.ra118.004672.
Canniffe, Daniel P., Thweatt, Jennifer L., Gomez Maqueo Chew, Aline, Hunter, C. Neil, and Bryant, Donald A. Mon . "A paralog of a bacteriochlorophyll biosynthesis enzyme catalyzes the formation of 1,2-dihydrocarotenoids in green sulfur bacteria". United States. doi:10.1074/jbc.ra118.004672. https://www.osti.gov/servlets/purl/1547337.
@article{osti_1547337,
title = {A paralog of a bacteriochlorophyll biosynthesis enzyme catalyzes the formation of 1,2-dihydrocarotenoids in green sulfur bacteria},
author = {Canniffe, Daniel P. and Thweatt, Jennifer L. and Gomez Maqueo Chew, Aline and Hunter, C. Neil and Bryant, Donald A.},
abstractNote = {Chlorobaculum tepidum, a green sulfur bacterium, utilizes chlorobactene as its major carotenoid, and this organism also accumulates a reduced form of this monocyclic pigment, 1′,2′-dihydrochlorobactene. The protein catalyzing this reduction is the last unidentified enzyme in the biosynthetic pathways for all of the green sulfur bacterial pigments utilized for photosynthesis. The genome of C. tepidum contains two paralogous genes encoding members of the FixC family of flavoproteins: bchP, which has been shown to encode an enzyme of bacteriochlorophyll biosynthesis; and bchO, for which a function has not been assigned. Here we demonstrate that a bchO mutant is unable to synthesize 1′,2′-dihydrochlorobactene, and when bchO is heterologously expressed in a neurosporene-producing mutant of the purple bacterium, Rhodobacter sphaeroides, the encoded protein is able to catalyze the formation of 1,2-dihydroneurosporene, the major carotenoid of the only other organism reported to synthesize 1,2-dihydrocarotenoids, Blastochloris viridis. Identification of this enzyme completes the pathways for the synthesis of photosynthetic pigments in Chlorobiaceae, and accordingly and consistent with its role in carotenoid biosynthesis, we propose to rename the gene cruI. Importantly, the absence of cruI in B. viridis indicates that a second 1,2-carotenoid reductase, which is structurally unrelated to CruI (BchO), must exist in nature. The evolution of this carotenoid reductase in green sulfur bacteria is discussed herein.},
doi = {10.1074/jbc.ra118.004672},
journal = {Journal of Biological Chemistry},
number = [39],
volume = [293],
place = {United States},
year = {2018},
month = {8}
}

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