ANRV322-MI61-15 ARI 6 August 2007 17:14 Postgenomic Adventures ∗ with Rhodobacter sphaeroides Chris Mackenzie, Jesus M. Eraso, Madhusudan Choudhary, Jung Hyeob Roh, Xiaohua Zeng, Patrice Bruscella, Agnes´ Puskas,´ and Samuel Kaplan Department of Microbiology and Molecular Genetics, University of Texas Health Science Center, Houston, Texas 77030; email: [email protected], [email protected], [email protected], [email protected], [email protected], [email protected], [email protected], [email protected] by Sam Houston State University on 07/28/10. For personal use only. Annu. Rev. Microbiol. 2007. 61:283–307 Key Words Annu. Rev. Microbiol. 2007.61:283-307. Downloaded from arjournals.annualreviews.org First published online as a Review in Advance on microarray, proteomics, gene-regulation, genome architecture, June 18, 2007 evolution The Annual Review of Microbiology is online at micro.annualreviews.org Abstract This article’s doi: This review describes some of the recent highlights taken from the 10.1146/annurev.micro.61.080706.093402 studies of Rhodobacter sphaeroides 2.4.1. The review is not intended Copyright c 2007 by Annual Reviews. to be comprehensive, but to reflect the bias of the authors as to how All rights reserved the availability of a sequenced and annotated genome, a gene-chip, 0066-4227/07/1013-0283$20.00 and proteomic profile as well as comparative genomic analyses can ∗ All authors contributed equally to this work. direct the progress of future research in this system. 283 ANRV322-MI61-15 ARI 6 August 2007 17:14 INTRODUCTION Contents The purple nonsulfur photosynthetic INTRODUCTION................. 284 Eubacterium, Rhodobacter sphaeroides 2.4.1 STRUCTURE AND FUNCTION. 284 (ATCC number BAA-808), belongs to the Structure and Function of the α-3 subgroup of the Proteobacteria and Photosynthetic Apparatus ...... 284 is metabolically highly versatile. It grows The Proteomic Analysis of by either aerobic or anaerobic respiration, R. sphaeroides .................. 285 photosynthesis, or fermentation. Organic COMMUNITY LIVING AND compounds are used as both a source of MOBILITY...................... 286 carbon and reductant for photoheterotrophic Quorum Sensing ................. 286 and chemoheterotrophic growth, with car- Motility.......................... 286 bon dioxide used as the sole carbon source MICROARRAY DATA .............. 287 under autotrophic growth conditions (89). Transcriptome Analysis of Hydrogen can be used as the source of reduc- R. sphaeroides 2.4.1 Using the ing power for photoautotrophic or chemoau- Affymetrix GeneChip.......... 287 totrophic growth (118). R. sphaeroides 2.4.1 GENE REGULATION ............. 289 can also utilize dinitrogen as the sole source Substitutive Global Regulators: of organic nitrogen. The ecological niche of Who Gets the Job Done in R. sphaeroides is a measure of its ability to pho- R. sphaeroides?................. 289 toassimilate low-molecular-weight organic E. coli Global Regulators Not products into cell material in the presence of Found in R. sphaeroides ......... 289 light or under conditions of oxygen limitation One- and Two-Component Signal and anaerobiosis (89). Although R. sphaeroides Transduction Systems in grows under conditions of high O2 tension, it R. sphaeroides .................. 290 appears to be best suited to microaerophilic The Prr Two-Component System conditions, allowing the organism to easily of R. sphaeroides ................ 291 transition between chemotrophic and pho- Global Regulatory Proteins ....... 292 totrophic growth. Movement is carried out FnrL ............................ 292 by a single subpolar flagellum. PpsR and the AppA-PpsR Antirepressor/Repressor System........................ 293 STRUCTURE AND FUNCTION GENOME ARCHITECTURE ..... 294 by Sam Houston State University on 07/28/10. For personal use only. Structure and Function of the Complex Genome Organization of Photosynthetic Apparatus R. sphaeroides .................. 294 The formation, function, regulation, and Annu. Rev. Microbiol. 2007.61:283-307. Downloaded from arjournals.annualreviews.org Reviewing the Process of Bacterial Cell Division: Multiple structure of the photosynthetic apparatus Chromosomes................. 294 have been well described over several years. Multiple Chromosomes Facilitate In response to decreasing oxygen tensions, Genetic Diversity ............. 295 R. sphaeroides develops intracytoplasmic mem- THE EVOLUTION branes (ICM), which are invaginations of the cytoplasmic membrane. The ICM contains OF R. sphaeroides?................ 295 the photosynthetic apparatus including the R. sphaeroides and the Tree of Life........................... 295 pigment protein complexes and the photosyn- An Evolutionary Mechanism? ..... 298 thetic electron carriers (123). After the isola- ˚ EPILOGUE ........................ 299 tion of chromatophores (sealed 50 A vesicles produced by pinching off the ICM) was first 284 Mackenzie et al. ANRV322-MI61-15 ARI 6 August 2007 17:14 reported (95), numerous studies have focused Atomic force microscopy has developed on examining the structure and function of into a powerful tool, generating high- their components. This led to breakthroughs resolution images of native ICM (3, 44, 96, ICM: in the 1980s and 1990s that defined the struc- 97). The ICM is composed of numerous intracytoplasmic ture and function of the reaction center (RC) photosynthetic domains in which linear ar- membrane and the light-harvesting (LH) complexes as rays of dimeric LH2 and LH1-RC-PufX Reaction center well as details of the primary photochemistry are clustered and arranged. The peripheral (RC): a of photosynthesis. A high-resolution struc- LH2 complexes are either grouped as 10–20 pigment-protein ture of the RC from R. sphaeroides (26) has molecules to form light-capture domains that structure found in demonstrated that the RC consists of three are directly associated with linear arrays of the membrane where photons of light are major subunits: L, M, and H. Both L and M dimers of core complexes (RC-LH1-Puf X), trapped and their have five-transmembrane domains and their or are clustered outside these arrays, with no energy converted orientation within the membranes were de- direct contact of these arrays to the core com- into a chemical form scribed as well as the path for electron flow plexes. However, where are the F0F1 ATP LH: light harvesting (81) and proton movement (83–86). The RC synthase and other components of the cyclic PS: photosynthesis is surrounded by the core antenna complex electron carriers, such as the bc1 complex? or photosynthetic LH1 to form the so-called LH1-RC-PufX Numerous biochemical and recent proteomic Proteomics: the core complex, with a fixed ratio of approxi- studies (17, 29) have confirmed that these pro- global study, often at mately 12:1 to 15:1. The LH2 complex sur- teins are present in the ICM. different times and rounds the LH1 complex and the ratio of LH2 under different to LH1 is variable, with the stoichiometry conditions, of the structure, function, changing in inverse proportion to the incident The Proteomic Analysis of R. sphaeroides and expression of light intensity via the differential regulation of proteins in a cell the two LH component types (56). See the fol- In recent proteomic studies, peptide mass fin- lowing references for details on the process of gerprinting was widely used to identify pro- light capture and energy transduction in the teins from sample mixtures (16). The accurate photosynthesis (PS) complex and the gener- mass and time tag approach has been utilized ation of ATP and proton motive force (pmf ) to identify various proteins and their subcel- (12, 112, 113). lular localization in aerobically and photosyn- In R. sphaeroides, the photosynthetic thetically grown R. sphaeroides (9, 10). A to- and respiratory pathways share a common tal of 8300 peptides were identified with high electron transfer chain. Oxygen represses bac- confidence (>0.7) and 1514 proteins (35% of teriochlorophyll and carotenoid (Crt) biosyn- proteins encoded by the genome) were se- by Sam Houston State University on 07/28/10. For personal use only. thesis and prevents the formation of the pho- quenced by matching the genome data of R. tosynthetic complexes. However, cytochrome sphaeroides 2.4.1. Of the proteins predicted to bc1 and cytochrome c2 remain, and respiratory be localized in a unique subcellular fraction Annu. Rev. Microbiol. 2007.61:283-307. Downloaded from arjournals.annualreviews.org electron transfer can use these carriers to by the program PSORTb, 81% agree with the transfer electrons to the cytochrome aa3 proteomic analysis. terminal oxidase, which has a low affinity for The proteomics approach has been uti- oxygen and is induced by increasing oxygen lized to analyze the protein components tension (68). Cytochrome cbb3 has a high affin- of intracytoplasmic vesicles, an initial re- ity for oxygen and is functional under low oxy- sult coming from purified ICM vesi- gen tension (77, 124). The presence of the cbb3 cles of Rhodopseudomonas palustris (28). In in the ICM, reported in a recent proteomic R. sphaeroides 2.4.1, the ICM vesicles con- study, is in accordance with its role under tain 609 proteins identified by match- low oxygen tension (X. Zeng, J.H. Roh, S.J. ing the annotation data obtained from Callister, C.L. Tavano, T.J. Donohue, M.S. the genome project of R. sphaeroides 2.4.1 Lipton & S. Kaplan, manuscript submitted). (http://www.rhodobacter.org/),