1887

Chapter 7 : Rickettsial Physiology and Metabolism in the Face of Reductive Evolution

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Rickettsial Physiology and Metabolism in the Face of Reductive Evolution, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817336/9781555816773_Chap07-1.gif /docserver/preview/fulltext/10.1128/9781555817336/9781555816773_Chap07-2.gif

Abstract:

One of the major emphases of the author's research program is to understand how obligate intracytoplasmic growth has affected the physiology of . This chapter discusses metabolism and reductive evolution from the pathogenic rickettsia's point of view. Rapid advances in sequencing technologies have contributed to the ever-expanding availability of genome sequence information. This has significantly augmented our understanding of the factors that influence virulence and shape pathogen evolution at the genome level. The chapter summarizes the studies describing rickettsial physiology and metabolism before 1998, when the first rickettsial genome sequence became available. It provides insight into some of the key experiments that guided the field during a productive period in rickettsial research. The adenosine triphosphate (ATP)/adenosine diphosphate (ADP) translocase is the best-characterized rickettsial transport system. It is well established that the ATP/ADP translocase functions via an obligate exchange antiport mechanism and thus requires the presence of substrate on both sides of the membrane to catalyze transport. Studies examining the physiology of rickettsiae that are growing intracellularly have contributed much to the understanding of rickettsia-host interactions. The chapter discusses how obligate intracellular growth has affected the rickettsia's capacity for gene regulation. As a final facet of rickettsial gene regulation, transcriptional termination is also explained in the chapter.

Citation: Audia J. 2012. Rickettsial Physiology and Metabolism in the Face of Reductive Evolution, p 221-242. In Palmer G, Azad A (ed), Intracellular Pathogens II: . ASM Press, Washington, DC. doi: 10.1128/9781555817336.ch7

Key Concept Ranking

Acetyl Coenzyme A
0.5083333
DNA Synthesis
0.4785676
Fatty Acid Biosynthesis
0.44948268
0.5083333
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Rickettsial energy parasitism. The ATP/ADP translocase (Tlc1) functions via an obligate exchange antiport mechanism that allows the obligate intracytoplasmic rickettsia to equilibrate its adenylate energy charge with that of the host as a system to transport high-energy phosphate. The rickettsial cytoplasm is shaded gray, the solid line represents the bacterial inner membrane where the Tlc1 protein (dark gray box) resides, and the dashed line represents the bacterial outer membrane. doi:10.1128/9781555817336.ch7.f1

Citation: Audia J. 2012. Rickettsial Physiology and Metabolism in the Face of Reductive Evolution, p 221-242. In Palmer G, Azad A (ed), Intracellular Pathogens II: . ASM Press, Washington, DC. doi: 10.1128/9781555817336.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

A model of reductive evolution. Panel A shows the facultative intracellular protorickettsia that possesses a typical de novo biosynthetic pathway in which rE1 denotes protorickettsial enzyme 1 and rE2 denotes protorickettsial enzyme 2. This pathway produces an essential metabolic end product. The same enzymatic pathway exists in the ancestral host cell cytoplasm, with the corresponding enzymes denoted as hE1 and hE2. This protorickettsia is not dependent on host cell metabolism for growth. Panel B shows that the obligate intracellular protorickettsia has acquired a transport system for a host cell metabolic end product (black box in the rickettsial inner membrane). The acquisition of this end product transporter has facilitated the loss of the corresponding rickettsial de novo biosynthetic pathway, as denoted by the absence of rE1 and rE2 in the protorickettsial cytoplasm. doi:10.1128/9781555817336.ch7.f2

Citation: Audia J. 2012. Rickettsial Physiology and Metabolism in the Face of Reductive Evolution, p 221-242. In Palmer G, Azad A (ed), Intracellular Pathogens II: . ASM Press, Washington, DC. doi: 10.1128/9781555817336.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Annotated fatty acid and phospholipid biosynthetic pathways. The components of these pathways that are annotated in the genome are denoted in italics with an asterisk and shaded gray. The lack of a classical bacterial four-subunit ACC enzyme complex is highlighted with a box around that part of the pathway. The large black arrows highlight the annotated G3P transporter (GlpT) and the annotated G3P dehydrogenase (GpsA). doi:10.1128/9781555817336.ch7.f3

Citation: Audia J. 2012. Rickettsial Physiology and Metabolism in the Face of Reductive Evolution, p 221-242. In Palmer G, Azad A (ed), Intracellular Pathogens II: . ASM Press, Washington, DC. doi: 10.1128/9781555817336.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Rickettsiae possess dual G3P acquisition pathways. The rickettsiae are able to directly transport the end product of a host metabolic pathway produced by the enzymatic activities of hE1 and hE2 using the end product transporter (black box in the rickettsial inner membrane). In addition, rickettsiae are able to transport substrate B from the host cell cytoplasm using the substrate B transporter (gray box in the rickettsial inner membrane). As a consequence of evolving the capacity for substrate B transport, the rickettsiae rE2 enzyme has been conserved and functions to synthesize a second source of the end product. doi:10.1128/9781555817336.ch7.f4

Citation: Audia J. 2012. Rickettsial Physiology and Metabolism in the Face of Reductive Evolution, p 221-242. In Palmer G, Azad A (ed), Intracellular Pathogens II: . ASM Press, Washington, DC. doi: 10.1128/9781555817336.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

Phylogenetic analysis of the rickettsial Tlc nucleotide transporters. A partial phylogenetic analysis was performed using the Clustal X program ( ). The unrooted tree diagram shows the clustering of the five Tlc proteins and indicates that gene duplication occurred before speciation. Abbreviations for spp.: Rp, ; Rt, ; Ra, ; Rf, ; Rm, ; Rs, ; Rc, ; Rr, . doi:10.1128/9781555817336.ch7.f5

Citation: Audia J. 2012. Rickettsial Physiology and Metabolism in the Face of Reductive Evolution, p 221-242. In Palmer G, Azad A (ed), Intracellular Pathogens II: . ASM Press, Washington, DC. doi: 10.1128/9781555817336.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6
FIGURE 6

A summary of the known properties of the Tlc family of nucleotide transporters. The Tlc transporters are shown in the rickettsial inner membrane. The question marks denote that substrates have not been identified for Tlc2 and Tlc3. Tlc1 is an obligate exchange antiporter. Tlc5 is an energy-dependent transporter. The energetics of Tlc4 are not yet known. doi:10.1128/9781555817336.ch7.f6

Citation: Audia J. 2012. Rickettsial Physiology and Metabolism in the Face of Reductive Evolution, p 221-242. In Palmer G, Azad A (ed), Intracellular Pathogens II: . ASM Press, Washington, DC. doi: 10.1128/9781555817336.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555817336.chap7
1. Alexeyev, M. F.,, and H. H. Winkler. 1999. Membrane topology of the Rickettsia prowazekii ATP/ADP translocase reported by novel dual pho-lac reporters. J. Mol. Biol. 285: 1503 1513.PubMed CrossRef
2. Andersson, J. O.,, and S. G. E. Andersson. 1999. Insights into the evolutionary process of genome degradation. Curr. Opin. Genet. Dev. 9: 664 671.PubMed
3. Andersson, J. O.,, and S. G. E. Andersson. 2001. Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes. Mol. Biol. Evol. 18: 829 839.PubMed
4. Andersson, S. G. E.,, A. Zomorodipour,, J. O. Andersson,, T. Sicheritz-Pontén,, U. C. M. Alsmark,, R. M. Podowdki,, A. K. Naslund,, A.-S. Eriksson,, H. H. Winkler,, and C. G. Kurland. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396: 133 140.PubMed CrossRef
5. Atkinson, D. E. 1969. Regulation of enzyme function. Annu. Rev. Microbiol. 23: 47 68.
6. Atkinson, W. H.,, and H. H. Winkler. 1989. Permeability of Rickettsia prowazekii to NAD. J. Bacteriol. 171: 761 766.PubMed
7. Audia, J. P.,, M. C. Patton,, and H. H. Winkler. 2008. DNA microarray analysis of the heat shock transcriptome of the obligate intracytoplasmic pathogen Rickettsia prowazekii. Appl. Environ. Microbiol. 74: 7809 7812.PubMed CrossRef
8. Audia, J. P.,, and H. H. Winkler. 2006. Study of the five Rickettsia prowazekii proteins annotated as ATP/ADP translocases (Tlc): only Tlc1 transports ATP/ADP, while Tlc4 and Tlc5 transport other ribonucleotides. J. Bacteriol. 188: 6261 6268.PubMed CrossRef
9. Austin, F. E.,, J. Turco,, and H. H. Winkler. 1987. Rickettsia prowazekii requires host cell serine and glycine for growth. Infect. Immun. 55: 240 244.PubMed
10. Austin, F. E.,, and H. H. Winkler. 1988a. Proline incorporation into protein by Rickettsia prowazekii during growth in Chinese hamster ovary (CHO-K1) cells. Infect. Immun. 56: 3167 3172.PubMed
11. Austin, F. E.,, and H. H. Winkler,. 1988b. Relationship of rickettsial physiology and composition to the Rickettsia-host cell interaction, p. 29 50. In D. H. Walker (ed.), Biology of Rickettsial Diseases, vol. 2. CRC Press, Boca Raton, FL.
12. Baldridge, G. D.,, N. Y. Burkhardt,, R. F. Felsheim,, T. J. Kurtti,, and U. G. Munderloh. 2008. Plasmids of the pRM/pRF family occur in diverse Rickettsia species. Appl. Environ. Microbiol. 74: 645 652.PubMed CrossRef
13. Borchert, S.,, J. Harborth,, D. Schunemann,, P. Hoferichter,, and H. W. Heldt. 1993. Studies of the enzymic capacities and transport properties of pea root plastids. Plant Physiol. 101: 303 312.PubMed
14. Bovarnick, M. R. 1956. Phosphorylation accompanying the oxidation of glutamate by the Madrid E strain of typhus rickettsiae. J. Biol. Chem. 220: 353 361.PubMed
15. Bovarnick, M. R.,, and E. G. Allen. 1957a. Reversible inactivation of the toxicity and hemolytic activity of typhus rickettsiae by starvation. J. Bacteriol. 74: 637 645.PubMed
16. Bovarnick, M. R.,, and E. G. Allen. 1957b. Reversible inactivation of typhus rickettsiae at 0°C. J. Bacteriol. 73: 56 62.PubMed
17. Bovarnick, M. R.,, E. G. Allen,, and G. Pagan. 1953. The influence of diphosphopyridine nucleotide on the stability of typhus rickettsiae. J. Bacteriol. 66: 671 675.PubMed
18. Bovarnick, M. R.,, and J. C. Miller. 1949. Oxidation and transamination of glutamate by typhus rickettsiae. J. Biol. Chem. 184: 661 676.PubMed
19. Bovarnick, M. R.,, and L. Schneider. 1960. Role of adenosine triphosphate in the hemolysis of sheep erythrocytes by typhus rickettsiae. J. Bacteriol. 80: 344 354.PubMed
20. Burgdorfer, W. 1975. A review of Rocky Mountain spotted fever (tick-borne typhus), its agent, and its tick vectors in the United States. J. Med. Entomol. 12: 269 278.PubMed
21. Cai, J.,, R. R. Speed,, and H. H. Winkler. 1991. Reduction of ribonucleotides by the obligate intracytoplasmic bacterium, Rickettsia prowazekii. J. Bacteriol. 173: 1471 1477.PubMed
22. Cai, J.,, and H. H. Winkler. 1996. Transcriptional regulation in the obligate intracytoplasmic bacterium Rickettsia prowazekii. J. Bacteriol. 178: 5543 5545.PubMed
23. Cai, J.,, and H. H. Winkler. 1997. Transcriptional regulation of the gltA and tlc genes in Rickettsia prowazekii growing in a respiration-deficient host cell. Acta Virol. 41: 285 288.PubMed
24. Chuakrut, S.,, H. Arai,, M. Ishii,, and Y. Igarashi. 2003. Characterization of a bifunctional archaeal acyl coenzyme A carboxylase. J. Bacteriol. 185: 938 947.PubMed
25. Ding, H.-F.,, and H. H. Winkler. 1990. Purification and partial characterization of the DNA-dependent RNA polymerase from Rickettsia prowazekii. J. Bacteriol. 172: 5624 5630.PubMed
26. Ding, H.-F.,, and H. H. Winkler. 1993. Characterization of the DNA-melting function of the Rickettsia prowazekii RNA polymerase. J. Biol. Chem. 268: 3897 3902.PubMed
27. Ding, H.-F.,, and H. H. Winkler. 1994. The molar ratio of σ 73 to core polymerase in the obligate intracellular bacterium, Rickettsia prowazekii. Mol. Microbiol. 11: 869 873.PubMed CrossRef
28. Dreher-Lesnick, S. M.,, S. M. Ceraul,, M. S. Rahman,, and A. F. Azad. 2008. Genome-wide screen for temperature-regulated genes of the obligate intracellular bacterium, Rickettsia typhi. BMC Microbiol. 8: 61.PubMed CrossRef
29. Driskell, L. O.,, A. M. Tucker,, H. H. Winkler,, and D. O. Wood. 2005. Rickettsial metK-encoded methionine adenosyltransferase expression in an Escherichia coli metK deletion strain. J. Bacteriol. 187: 5719 5722.PubMed CrossRef
30. Ellison, D. W.,, T. R. Clark,, D. E. Sturdevant,, K. Virtaneva,, and T. Hackstadt. 2009. Limited transcriptional responses of Rickettsia rickettsii exposed to environmental stimuli. PLoS One 4: e5612.PubMed CrossRef
31. Ellison, D. W.,, T. R. Clark,, D. E. Sturdevant,, K. Virtaneva,, S. F. Porcella,, and T. Hackstadt. 2008. Genomic comparison of virulent Rickettsia rickettsii Sheila Smith and avirulent Rickettsia rickettsii Iowa. Infect. Immun. 76: 542 550.PubMed CrossRef
32. Fairlamb, A. H.,, and F. R. Opperdoes,. 1986. Carbohydrate metabolism in African trypanosomes, with special reference to the glycosome, p. 183 224. In M. J. Morgan (ed.), Carbohydrate Metabolism in Cultured Cells. Plenum Publishing Corporation, New York, NY.
33. Felsheim, R. F.,, T. J. Kurtti,, and U. G. Munderloh. 2009. Genome sequence of the endosymbiont Rickettsia peacockii and comparison with virulent Rickettsia rickettsii: identification of virulence factors. PLoS One 4: e8361.PubMed CrossRef
34. Fournier, P. E.,, K. El Karkouri,, Q. Leroy,, C. Robert,, B. Giumelli,, P. Renesto,, C. Socolovschi,, P. Parola,, S. Audic,, and D. Raoult. 2009. Analysis of the Rickettsia africae genome reveals that virulence acquisition in Rickettsia species may be explained by genome reduction. BMC Genomics 10: 166.PubMed CrossRef
35. Frohlich, K. M.,, R. A. Roberts,, N. A. Housley,, and J. P. Audia. 2010. Rickettsia prowazekii uses an sn-glycerol-3-phosphate dehydrogenase and a novel dihydroxyacetone phosphate transport system to supply triose phosphate for phospholipid biosynthesis. J. Bacteriol. 192: 4281 4288.PubMed CrossRef
36. Gentry, D. R.,, and M. Cashel. 1996. Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol. Microbiol. 19: 1373 1384.PubMed CrossRef
37. Greub, G.,, and D. Raoult. 2003. History of the ADP/ATP-translocase-encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl. Environ. Microbiol. 69: 5530 5535.PubMed CrossRef
38. Gudima, O. S. 1982. Reproduction of vaccine and virulent Rickettsia prowazeki strains in continuous cell lines at different temperatures. Acta Virol. 26: 390 394.PubMed
39. Hackstadt, T. 1996. The biology of rickettsiae. Infect. Agents Dis. 5: 127 143.
40. Hügler, M.,, R. S. Krieger,, M. Jahn,, and G. Fuchs. 2003. Characterization of acetyl-CoA/propionyl-CoA carboxylase in Metallosphaera sedula. Carboxylating enzyme in the 3-hydroxypropionate cycle for autotrophic carbon fixation. Eur. J. Biochem. 270: 736 744.PubMed
41. La, M. V.,, P. Francois,, C. Rovery,, S. Robineau,, P. Barbry,, J. Schrenzel,, D. Raoult,, and P. Renesto. 2007. Development of a method for recovering rickettsial RNA from infected cells to analyze gene expression profiling of obligate intracellular bacteria. J. Microbiol. Methods 71: 292 297.PubMed CrossRef
42. Larkin, M. A.,, G. Blackshields,, N. P. Brown,, R. Chenna,, P. A. McGettigan,, H. McWilliam,, F. Valentin,, I. M. Wallace,, A. Wilm,, R. Lopez,, J. D. Thompson,, T. J. Gibson,, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947 2948.PubMed CrossRef
43. Moliner, C.,, P. E. Fournier,, and D. Raoult. 2010. Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol. Rev. 34: 281 294.PubMed CrossRef
44. Moulder, J. W. 1962. The Biochemistry of Intracellular Parasitism. University of Chicago Press, Chicago, IL.
45. Ogata, H.,, B. La Scola,, S. Audic,, P. Renesto,, G. Blanc,, C. Robert,, P. E. Fournier,, J. M. Claverie,, and D. Raoult. 2006. Genome sequence of Rickettsia bellii illuminates the role of amoebae in gene exchanges between intracellular pathogens. PLoS Genet. 2: e76.PubMed CrossRef
46. Pallen, M. J.,, and B. W. Wren. 2007. Bacterial pathogenomics. Nature 449: 835 842.PubMed CrossRef
47. Pang, H.,, and H. H. Winkler. 1993. Copy number of the 16S ribosomal RNA gene in Rickettsia prowazekii. J. Bacteriol. 175: 3893 3896.
48. Pang, H.,, and H. H. Winkler. 1994. The concentrations of stable RNA and ribosomes in Rickettsia prowazekii. Mol. Microbiol. 12: 115 120.PubMed CrossRef
49. Paulsen, I. T.,, L. Nguyen,, M. K. Sliwinski,, R. Rabus,, and M. H. Saier, Jr. 2000. Microbial genome analyses: comparative transport capabilities in eighteen prokaryotes. J. Mol. Biol. 301: 75 100.PubMed CrossRef
50. Phibbs, P. V., Jr.,, and H. H. Winkler,. 1981. Regulatory properties of partially purified enzymes of the tricarboxylic acid cycle of Rickettsia prowazekii, p. 421 430. In W. Burgdorfer, and R. Anacker (ed.), Rickettsiae and Rickettsial Diseases. Academic Press, New York, NY.
51. Phibbs, P. V., Jr.,, and H. H. Winkler. 1982. Regulatory properties of citrate synthase from Rickettsia prowazekii. J. Bacteriol. 149: 718 725.PubMed
52. Plano, G. V.,, and H. H. Winkler. 1991. Identification and initial topological analysis of the Rickettsia prowazekii ATP/ADP translocase. J. Bacteriol. 173: 3389 3396.PubMed
53. Quick, W. P.,, and H. E. Neuhaus. 1996. Evidence for two types of phosphate translocators in sweet-pepper ( Capsicum annum L.) fruit chromoplasts. Biochem. J. 320: 7 10.PubMed
54. Ralser, M.,, M. M. Wamelink,, A. Kowald,, B. Gerisch,, G. Heeren,, E. A. Struys,, E. Klipp,, C. Jakobs,, M. Breitenbach,, H. Lehrach,, and S. Krobitsch. 2007. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J. Biol. 6: 10.PubMed CrossRef
55. Ralser, M.,, M. M. Wamelink,, S. Latkolik,, E. E. Jansen,, H. Lehrach,, and C. Jakobs. 2009. Metabolic reconfiguration precedes transcriptional regulation in the antioxidant response. Nat. Biotechnol. 27: 604 605.PubMed CrossRef
56. Ramm, L. E.,, and H. H. Winkler. 1973. Rickettsial hemolysis: effect of metabolic inhibitors upon hemolysis and adsorption. Infect. Immun. 7: 550 555.PubMed
57. Renesto, P.,, C. Rovery,, J. Schrenzel,, Q. Leroy,, A. Huyghe,, W. Li,, H. Lepidi,, P. Francois,, and D. Raoult. 2008. Rickettsia conorii transcriptional response within inoculation eschar. PLoS One 3: e3681.PubMed CrossRef
58. Rovery, C.,, P. Renesto,, N. Crapoulet,, K. Matsumoto,, P. Parola,, H. Ogata,, and D. Raoult. 2005. Transcriptional response of Rickettsia conorii exposed to temperature variation and stress starvation. Res. Microbiol. 156: 211 218.PubMed CrossRef
59. Saier, M. H., Jr.,, C. V. Tran,, and R. D. Barabote. 2006. TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res. 34( Database issue): D181 D186.PubMed CrossRef
60. Shaw, E. I.,, G. L. Marks,, H. H. Winkler,, and D. O. Wood. 1997. Transcriptional characterization of the Rickettsia prowazekii major macromolecular synthesis operon. J. Bacteriol. 179: 6448 6452.PubMed
61. Sicheritz-Pontén, T.,, C. G. Kurland,, and S. G. E. Andersson. 1998. A phylogenetic analysis of the cytochrome b and cytochrome c oxidase I genes supports an origin of mitochondria from within the Rickettsiaceae. Biochim. Biophys. Acta 1365: 545 551.PubMed
62. Smith, D. K.,, and H. H. Winkler. 1979. Separation of inner and outer membranes of Rickettsia prowazekii and characterization of their polypeptide compositions. J. Bacteriol. 137: 963 971.PubMed
63. Stork, E.,, and C. L. Wisseman, Jr. 1976. Growth of Rickettsia prowazeki in enucleated cells. Infect. Immun. 13: 1743 1748.PubMed
64. Tjaden, J.,, H. H. Winkler,, C. Schwöppe,, M. van der Laan,, T. Möhlmann,, and H. E. Neuhaus. 1999. Two nucleotide transport proteins in Chlamydia trachomatis: one for net nucleoside triphosphate uptake and the other for transport of energy. J. Bacteriol. 181: 1196 1202.PubMed
65. Trentmann, O.,, B. Jung,, H. E. Neuhaus,, and I. Haferkamp. 2008. Nonmitochondrial ATP/ADP transporters accept phosphate as third substrate. J. Biol. Chem. 283: 36486 36493.PubMed CrossRef
66. Tucker, A. M.,, H. H. Winkler,, L. O. Driskell,, and D. O. Wood. 2003. S-Adenosylmethionine transport in Rickettsia prowazekii. J. Bacteriol. 185: 3031 3035.PubMed CrossRef
67. Turco, J.,, and H. H. Winkler. 1989. Isolation of Rickettsia prowazekii with reduced sensitivity to gamma interferon. Infect. Immun. 57: 1765 1772.PubMed
68. Tzianabos, T.,, C. W. Moss,, and J. E. McDade. 1981. Fatty acid composition of rickettsiae. J. Clin. Microbiol. 13: 603 605.PubMed
69. Walker, T. S.,, and H. H. Winkler. 1978. Penetration of cultured mouse fibroblasts (L cells) by Rickettsia prowazekii. Infect. Immun. 22: 200 208.PubMed
70. Weiss, E.,, L. W. Newman,, R. Grays,, and A. E. Green. 1972. Metabolism of Rickettsia typhi and Rickettsia akari in irradiated L cells. Infect. Immun. 6: 50 57.PubMed
71. Wike, D. A.,, and W. Burgdorfer. 1972. Plaque formation in tissue cultures by Rickettsia rickettsi isolated directly from whole blood and tick hemolymph. Infect. Immun. 6: 736 738.PubMed
72. Wike, D. A.,, R. A. Ormsbee,, G. Tallent,, and M. G. Peacock. 1972. Effects of various suspending media on plaque formation by rickettsiae in tissue culture. Infect. Immun. 6: 550 556.PubMed
73. Williams, J. C.,, and E. Weiss. 1978. Energy metabolism of Rickettsia typhi: pools of adenine nucleotides and energy charge in the presence and absence of glutamate. J. Bacteriol. 134: 884 892.PubMed
74. Winkler, H. H. 1976. Rickettsial permeability: an ADP-ATP transport system. J. Biol. Chem. 251: 389 396.PubMed
75. Winkler, H. H. 1982. Rickettsiae: intracytoplamic life. ASM News 48: 184 186.
76. Winkler, H. H. 1987. Protein and RNA synthesis by isolated Rickettsia prowazekii. Infect. Immun. 55: 2032 2036.PubMed
77. Winkler, H. H. 1990. Rickettsia species (as organisms). Annu. Rev. Microbiol. 44: 131 153.PubMed CrossRef
78. Winkler, H. H.,, R. Daugherty,, and F. Hu. 1999. Rickettsia prowazekii transports UMP and GMP, but not CMP, as building blocks for RNA synthesis. J. Bacteriol. 181: 3238 3241.PubMed
79. Winkler, H. H.,, and R. M. Daugherty. 1984. Regulatory role of phosphate and other anions in transport of ADP and ATP by Rickettsia prowazekii. J. Bacteriol. 160: 76 79.PubMed
80. Winkler, H. H.,, and R. M. Daugherty. 1986. Acquisition of glucose by Rickettsia prowazekii through the nucleotide intermediate uridine 5'-diphosphoglucose. J. Bacteriol. 167: 805 808.PubMed
81. Winkler, H. H.,, and E. T. Miller. 1978. Phospholipid composition of Rickettsia prowazeki grown in chicken embryo yolk sacs. J. Bacteriol. 136: 175 178.PubMed
82. Winkler, H. H.,, and H. E. Neuhaus. 1999. Non-mitochondrial adenylate transport: a plant plastid to obligate intracellular bacterium connection. Trends Biochem. Sci. 277: 64 68.
83. Wisseman, C. L., Jr.,, E. A. Edlinger,, A. D. Waddell,, and M. R. Jones. 1976. Infection cycle of Rickettsia rickettsii in chicken embryo and L-929 cells in culture. Infect. Immun. 14: 1052 1064.PubMed
84. Woodard, A.,, and D. O. Wood. 2011. Analysis of convergent gene transcripts in the obligate intracellular bacterium Rickettsia prowazekii. PLoS One 6: e16537.PubMed CrossRef
85. Wu, J.,, and J. Xie. 2009. Magic spot: (p) ppGpp. J. Cell. Physiol. 220: 297 302.PubMed CrossRef
86. Zahorchak, R. J.,, and H. H. Winkler. 1983. Transmembrane electrical potential in Rickettsia prowazekii and its relationship to lysine transport. J. Bacteriol. 153: 665 671.PubMed

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error