A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis

被引:129
作者
Anthony, JR [1 ]
Warczak, KL [1 ]
Donohue, TJ [1 ]
机构
[1] Univ Wisconsin, Dept Bacteriol, Madison, WI 53706 USA
关键词
sigma factor; reactive oxygen species; Rhodobacter sphaeroides; photochemistry; carotenoids;
D O I
10.1073/pnas.0502225102
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The ability of phototrophs to convert light into biological energy is critical for life on Earth. However, there can be deleterious consequences associated with this bioenergetic conversion, including the production of toxic byproducts. For example, singlet oxygen (O-1(2)) can be formed during photosynthesis by energy transfer from excited triplet-state chlorophyll pigments to O-2. By monitoring gene expression and growth in the presence of O-1(2), we show that the phototrophic bacterium Rhodobacter sphaeroides mounts a transcriptional response to this reactive oxygen species (ROS) that requires the alternative sigma factor, sigma(E). An increase in sigma(E) activity is seen when cells are exposed to O-1(2) generated either by photochemistry within the photosynthetic apparatus or the photosensitizer, methylene blue. Wavelengths of light responsible for the generating triplet-state chlorophyll pigments in the photosynthetic apparatus are sufficient for a sustained increase in sigma(E) activity. Continued exposure to O-1(2) is required to maintain this transcriptional response, and other ROS do not cause a similar increase in sigma(E)-dependent gene expression. When a sigma(E) mutant produces low levels of carotenoids, O-1(2) is bacteriocidal, suggesting that this response is essential for protecting cells from this ROS. In addition, global gene expression analysis identified approximate to 180 genes (approximate to 60 operons) whose RNA levels increase >= 3-fold in cells with increased sigma(E) activity. Gene products encoded by four newly identified sigma(E)-dependent operons are predicted to be involved in stress response, protecting cells from O-1(2) damage, or the conservation of energy.
引用
收藏
页码:6502 / 6507
页数:6
相关论文
共 60 条
[1]   Singlet molecular oxygen triggers the soxRS regulon of Escherichia coli [J].
Agnez-Lima, LF ;
Di Mascio, P ;
Demple, B ;
Menck, CFM .
BIOLOGICAL CHEMISTRY, 2001, 382 (07) :1071-1075
[2]   Interactions between the Rhodobacter sphaeroides ECF sigma factor, σE, and its anti-sigma factor, ChrR [J].
Anthony, JR ;
Newman, JD ;
Donohue, TJ .
JOURNAL OF MOLECULAR BIOLOGY, 2004, 341 (02) :345-360
[3]  
Anthony JR, 2003, METHOD ENZYMOL, V370, P54
[4]   Reactive oxygen species: Metabolism, oxidative stress, and signal transduction [J].
Apel, K ;
Hirt, H .
ANNUAL REVIEW OF PLANT BIOLOGY, 2004, 55 :373-399
[5]   Responses of the Rhodobacter sphaeroides transcriptome to blue light under semiaerobic conditions [J].
Braatsch, S ;
Moskvin, OV ;
Klug, G ;
Gomelsky, M .
JOURNAL OF BACTERIOLOGY, 2004, 186 (22) :7726-7735
[6]   EXPRESSION OF THE RHODOBACTER-SPHAEROIDES CYTOCHROME-C2 STRUCTURAL GENE [J].
BRANDNER, JP ;
MCEWAN, AG ;
KAPLAN, S ;
DONOHUE, TJ .
JOURNAL OF BACTERIOLOGY, 1989, 171 (01) :360-368
[7]  
Briviba K, 1997, BIOL CHEM, V378, P1259
[8]   INDUCTION OF THE PHOTOSYNTHETIC MEMBRANES OF RHODOPSEUDOMONAS-SPHAEROIDES - BIOCHEMICAL AND MORPHOLOGICAL-STUDIES [J].
CHORY, J ;
DONOHUE, TJ ;
VARGA, AR ;
STAEHELIN, LA ;
KAPLAN, S .
JOURNAL OF BACTERIOLOGY, 1984, 159 (02) :540-554
[9]   How carotenoids protect bacterial photosynthesis [J].
Cogdell, RJ ;
Howard, TD ;
Bittl, R ;
Schlodder, E ;
Geisenheimer, I ;
Lubitz, W .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES, 2000, 355 (1402) :1345-1349
[10]   HOW CAROTENOIDS FUNCTION IN PHOTOSYNTHETIC BACTERIA [J].
COGDELL, RJ ;
FRANK, HA .
BIOCHIMICA ET BIOPHYSICA ACTA, 1987, 895 (02) :63-79