Chapter 8 : : Carbon Metabolism and the Tick-Mammal Enzootic Cycle

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

Preview this chapter:
Zoom in

: Carbon Metabolism and the Tick-Mammal Enzootic Cycle, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818883/9781555818869_Chap08-1.gif /docserver/preview/fulltext/10.1128/9781555818883/9781555818869_Chap08-2.gif


is the spirochetal agent of Lyme disease, the most commonly reported arthropod-borne disease in the United States ( ). is a zoonotic pathogen that is maintained in a natural cycle involving mammalian reservoir hosts such as field mice, squirrels, and birds and an arthropod vector of the species ( ) ( Fig. 1 ). In the United States, the principal vector is , the common deer tick ( ). Because there is no transovarial transmission of , newly hatched larvae acquire the spirochete during their first blood meal on an infected mammalian host reservoir ( ). The spirochete is maintained in the midgut of the tick during molting to the nymphal stage. At this point, the spirochete is in a nonmotile state until the nymph begins to feed on the next mammalian host ( ). The spirochete then begins rapidly replicating in the feeding nymphal midgut, leaves the midgut and enters the hemolymph, from which the bacteria migrate to the salivary glands and are transmitted to the next mammalian host ( ) ( Fig. 1 ).

Citation: Corona A, Schwartz I. 2015. : Carbon Metabolism and the Tick-Mammal Enzootic Cycle, p 167-184. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0011-2014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

enzootic cycle. (1) Uninfected larva emerges from eggs. (2) Larval acquisition of during a blood meal on an infected reservoir host. (3) Infected fed larva molts to an unfed nymph. (4) Transmission of from a feeding nymph to an uninfected reservoir host during the nymphal blood meal. (5) Infected fed nymph molts to an adult. (6) Female and male adults mate on a large mammal (typically deer). The female adult feeds on the large mammal and lays eggs.

Citation: Corona A, Schwartz I. 2015. : Carbon Metabolism and the Tick-Mammal Enzootic Cycle, p 167-184. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0011-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

carbohydrate transporters. Schematic diagram indicates predicted or experimentally verified transport systems. numbers indicate gene locus in strain B31 ( ). Based on von Lackum and Stevenson ( ).

Citation: Corona A, Schwartz I. 2015. : Carbon Metabolism and the Tick-Mammal Enzootic Cycle, p 167-184. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0011-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

The glycolytic pathway and control of glycolytic flux during the enzootic cycle.

Citation: Corona A, Schwartz I. 2015. : Carbon Metabolism and the Tick-Mammal Enzootic Cycle, p 167-184. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0011-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Schematic diagram depicting reported regulatory circuits controlling glycerol and chitobiose utilization. Solid lines indicate interactions confirmed by studies; dashed lines indicate interactions observed only. Diagram is a summary of data from references , and .

Citation: Corona A, Schwartz I. 2015. : Carbon Metabolism and the Tick-Mammal Enzootic Cycle, p 167-184. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0011-2014
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Bacon RM,, Kugeler KJ,, Mead PS . 2008. Surveillance for Lyme disease—United States, 1992–2006. MMWR Surveill Summ 57 : 19.[PubMed]
2. Steere AC,, Grodzicki RL,, Kornblatt AN,, Craft JE,, Barbour AG,, Burgdorfer W,, Schmid GP,, Johnson E,, Malawista SE . 1983. The spirochetal etiology of Lyme disease. N Engl J Med 308 : 733740.[PubMed] [CrossRef]
3. Benach JL,, Bosler EM,, Hanrahan JP,, Coleman JL,, Habicht GS,, Bast TF,, Cameron DJ,, Ziegler JL,, Barbour AG,, Burgdorfer W,, Edelman R,, Kaslow RA . 1983. Spirochetes isolated from the blood of two patients with Lyme disease. N Engl J Med 308 : 740742.[PubMed] [CrossRef]
4. Levine JF,, Wilson ML,, Spielman A . 1985. Mice as reservoirs of the Lyme disease spirochete. Am J Trop Med Hyg 34 : 355360.[PubMed]
5. Tsao JI . 2009. Reviewing molecular adaptations of Lyme borreliosis spirochetes in the context of reproductive fitness in natural transmission cycles. Vet Res 40 : 36. [PubMed] [CrossRef]
6. Radolf JD,, Caimano MJ,, Stevenson B,, Hu LT . 2012. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat Rev Microbiol 10 : 8799.[PubMed] [CrossRef]
7. Magnarelli LA,, Anderson JF,, Fish D . 1987. Transovarial transmission of Borrelia burgdorferi in Ixodes dammini (Acari:Ixodidae). J Infect Dis 156 : 234236.[PubMed] [CrossRef]
8. Rollend L,, Fish D,, Childs JE . 2013. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: a summary of the literature and recent observations. Ticks Tick-borne Dis 4 : 4651.[PubMed] [CrossRef]
9. Dunham-Ems SM,, Caimano MJ,, Pal U,, Wolgemuth CW,, Eggers CH,, Balic A,, Radolf JD . 2009. Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J Clin Invest 119 : 36523665.[PubMed] [CrossRef]
10. De Silva AM,, Fikrig E . 1995. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am J Trop Med Hyg 53 : 397404.[PubMed]
11. Piesman J,, Schneider BS,, Zeidner NS . 2001. Use of quantitative PCR to measure density of Borrelia burgdorferi in the midgut and salivary glands of feeding tick vectors. J Clin Microbiol 39 : 41454148.[PubMed] [CrossRef]
12. Pappas CJ,, Iyer R,, Petzke MM,, Caimano MJ,, Radolf JD,, Schwartz I . 2011. Borrelia burgdorferi requires glycerol for maximum fitness during the tick phase of the enzootic cycle. PLoS Pathog 7 : e1002102. [PubMed] [CrossRef]
13. Steere AC,, Coburn J,, Glickstein L . 2004. The emergence of Lyme disease. J Clin Invest 113 : 10931101.[PubMed] [CrossRef]
14. Pal U,, Fikrig E, . 2010. Tick Interactions, p 279298. In Samuels DS,, Radolf JD (ed.), Borrelia: Molecular biology, host interaction and pathogenesis. Caister Academic Press, Norfolk, UK. [PubMed]
15. Shao L,, Devenport M,, Jacobs-Lorena M . 2001. The peritrophic matrix of hematophagous insects. Arch Insect Biochem Physiol 47 : 119125.[PubMed] [CrossRef]
16. Rohmer L,, Hocquet D,, Miller SI . 2011. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol 19 : 341348.[PubMed] [CrossRef]
17. Fraser CM,, Casjens S,, Huang WM,, Sutton GG,, Clayton R,, Lathigra R,, White O,, Ketchum KA,, Dodson R,, Hickey EK,, Gwinn M,, Dougherty B,, Tomb JF,, Fleischmann RD,, Richardson D,, Peterson J,, Kerlavage AR,, Quackenbush J,, Salzberg S,, Hanson M,, van VR,, Palmer N,, Adams MD,, Gocayne J,, Weidman J,, Utterback T,, Watthey L,, McDonald L,, Artiach P,, Bowman C,, Garland S,, Fuji C,, Cotton MD,, Horst K,, Roberts K,, Hatch B,, Smith HO,, Venter JC . 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi . Nature 390 : 580586.[PubMed] [CrossRef]
18. Casjens S,, Palmer N,, van VR,, Huang WM,, Stevenson B,, Rosa P,, Lathigra R,, Sutton G,, Peterson J,, Dodson RJ,, Haft D,, Hickey E,, Gwinn M,, White O,, Fraser CM . 2000. A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi . Mol Microbiol 35 : 490516.[PubMed] [CrossRef]
19. Brisson D,, Drecktrah D,, Eggers CH,, Samuels DS . 2012. Genetics of Borrelia burgdorferi . Annu Rev Genet 46 : 515536.[PubMed] [CrossRef]
20. Iyer R,, Kalu O,, Purser J,, Norris S,, Stevenson B,, Schwartz I . 2003. Linear and circular plasmid content in Borrelia burgdorferi clinical isolates. Infect Immun 71 : 36993706.[PubMed] [CrossRef]
21. Terekhova D,, Iyer R,, Wormser GP,, Schwartz I . 2006. Comparative genome hybridization reveals substantial variation among clinical isolates of Borrelia burgdorferi sensu stricto with different pathogenic properties. J Bacteriol 188 : 61246134.[PubMed] [CrossRef]
22. Casjens SR,, Mongodin EF,, Qiu WG,, Luft BJ,, Schutzer SE,, Gilcrease EB,, Huang WM,, Vujadinovic M,, Aron JK,, Vargas LC,, Freeman S,, Radune D,, Weidman JF,, Dimitrov GI,, Khouri HM,, Sosa JE,, Halpin RA,, Dunn JJ,, Fraser CM . 2012. Genome stability of Lyme disease spirochetes: comparative genomics of Borrelia burgdorferi plasmids. PLoS ONE 7 : e33280. [PubMed] [CrossRef]
23. Purser JE,, Norris SJ . 2000. Correlation between plasmid content and infectivity in Borrelia burgdorferi . Proc Natl Acad Sci U S A 97 : 1386513870.[PubMed] [CrossRef]
24. Purser JE,, Lawrenz MB,, Caimano MJ,, Howell JK,, Radolf JD,, Norris SJ . 2003. A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48 : 753764.[PubMed] [CrossRef]
25. Byram R,, Stewart PE,, Rosa P . 2004. The essential nature of the ubiquitous 26-kilobase circular replicon of Borrelia burgdorferi . J Bacteriol 186 : 35613569.[PubMed] [CrossRef]
26. Stewart PE,, Byram R,, Grimm D,, Tilly K,, Rosa PA . 2005. The plasmids of Borrelia burgdorferi: essential genetic elements of a pathogen. Plasmid 53 : 113.[PubMed] [CrossRef]
27. Grimm D,, Tilly K,, Bueschel DM,, Fisher MA,, Policastro PF,, Gherardini FC,, Schwan TG,, Rosa PA . 2005. Defining plasmids required by Borrelia burgdorferi for colonization of tick vector Ixodes scapularis (Acari: Ixodidae). J Med Entomol 42 : 676684.[PubMed] [CrossRef]
28. Chaconas G,, Kobryn K . 2010. Structure, function, and evolution of linear replicons in Borrelia . Annu Rev Microbiol 64 : 185202.[PubMed] [CrossRef]
29. Chaconas G,, Norris SJ . 2013. Peaceful coexistence amongst Borrelia plasmids: getting by with a little help from their friends? Plasmid 70 : 161167.[PubMed] [CrossRef]
30. Dulebohn DP,, Bestor A,, Rosa PA . 2013. Borrelia burgdorferi linear plasmid 28-3 confers a selective advantage in an experimental mouse-tick infection model. Infect Immun 81 : 29862996.[PubMed] [CrossRef]
31. Jewett MW,, Byram R,, Bestor A,, Tilly K,, Lawrence K,, Burtnick MN,, Gherardini F,, Rosa PA . 2007. Genetic basis for retention of a critical virulence plasmid of Borrelia burgdorferi . Mol Microbiol 66 : 975990.[PubMed] [CrossRef]
32. Gherardini F,, Boylan J,, Lawrence K,, Skare J, . 2010. Metabolism and Physiology of Borrelia , p 103138. In Samuels DS,, Radolf JD (ed.), Borrelia: Molecular biology, host interaction and pathogenesis. Caister Academic Press, Norfolk, UK.
33. Jewett MW,, Lawrence KA,, Bestor A,, Byram R,, Gherardini F,, Rosa PA . 2009. GuaA and GuaB are essential for Borrelia burgdorferi survival in the tick-mouse infection cycle. J Bacteriol 191 : 62316241.[PubMed] [CrossRef]
34. Tilly K,, Krum JG,, Bestor A,, Jewett MW,, Grimm D,, Bueschel D,, Byram R,, Dorward D,, Vanraden MJ,, Stewart P,, Rosa P . 2006. Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect Immun 74 : 35543564.[PubMed] [CrossRef]
35. Labandeira-Rey M,, Skare JT . 2001. Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect Immun 69 : 446455.[PubMed] [CrossRef]
36. Jewett MW,, Jain S,, Linowski AK,, Sarkar A,, Rosa PA . 2011. Molecular characterization of the Borrelia burgdorferi in vivo-essential protein PncA. Microbiology 157 : 28312840.[PubMed] [CrossRef]
37. Zhang JR,, Hardham JM,, Barbour AG,, Norris SJ . 1997. Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89 : 275285.[PubMed] [CrossRef]
38. Zhang JR,, Norris SJ . 1998. Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect Immun 66 : 36983704.[PubMed]
39. Norris SJ . 2006. Antigenic variation with a twist–the Borrelia story. Mol Microbiol 60 : 13191322.[PubMed] [CrossRef]
40. Kazmierczak MJ,, Wiedmann M,, Boor KJ . 2005. Alternative sigma factors and their roles in bacterial virulence. Microbiol Mol Biol Rev 69 : 527543.[PubMed] [CrossRef]
41. Beier D,, Gross R . 2006. Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9 : 143152.[PubMed] [CrossRef]
42. Hubner A,, Yang X,, Nolen DM,, Popova TG,, Cabello FC,, Norgard MV . 2001. Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN-RpoS regulatory pathway. Proc Natl Acad Sci U S A 98 : 1272412729.[PubMed] [CrossRef]
43. Yang XF,, Alani SM,, Norgard MV . 2003. The response regulator Rrp2 is essential for the expression of major membrane lipoproteins in Borrelia burgdorferi . Proc Natl Acad Sci U S A 100 : 1100111006.[PubMed] [CrossRef]
44. Caimano MJ,, Eggers CH,, Hazlett KR,, Radolf JD . 2004. RpoS is not central to the general stress response in Borrelia burgdorferi but does control expression of one or more essential virulence determinants. Infect Immun 72 : 64336445.[PubMed] [CrossRef]
45. Caimano MJ,, Eggers CH,, Gonzalez CA,, Radolf JD . 2005. Alternate sigma factor RpoS is required for the in vivo-specific repression of Borrelia burgdorferi plasmid lp54-borne ospA and lp6.6 genes. J Bacteriol 187 : 78457852.[PubMed] [CrossRef]
46. Dunham-Ems SM,, Caimano MJ,, Eggers CH,, Radolf JD . 2012. Borrelia burgdorferi requires the alternative sigma factor RpoS for dissemination within the vector during tick-to-mammal transmission. PLoS Pathog 8 : e1002532. [PubMed] [CrossRef]
47. Caimano MJ,, Iyer R,, Eggers CH,, Gonzalez C,, Morton EA,, Gilbert MA,, Schwartz I,, Radolf JD . 2007. Analysis of the RpoS regulon in Borrelia burgdorferi in response to mammalian host signals provides insight into RpoS function during the enzootic cycle. Mol Microbiol 65 : 11931217.[PubMed] [CrossRef]
48. Samuels DS . 2011. Gene regulation in Borrelia burgdorferi . Annu Rev Microbiol 65 : 479499.[PubMed] [CrossRef]
49. Ouyang Z,, Blevins JS,, Norgard MV . 2008. Transcriptional interplay among the regulators Rrp2, RpoN and RpoS in Borrelia burgdorferi . Microbiology 154 : 26412658.[PubMed] [CrossRef]
50. Blevins JS,, Xu H,, He M,, Norgard MV,, Reitzer L,, Yang XF . 2009. Rrp2, a sigma54-dependent transcriptional activator of Borrelia burgdorferi, activates rpoS in an enhancer-independent manner. J Bacteriol 191 : 29022905.[PubMed] [CrossRef]
51. Ouyang Z,, Narasimhan S,, Neelakanta G,, Kumar M,, Pal U,, Fikrig E,, Norgard MV . 2012. Activation of the RpoN-RpoS regulatory pathway during the enzootic life cycle of Borrelia burgdorferi . BMC Microbiol 12 : 44. [PubMed] [CrossRef]
52. Smith AH,, Blevins JS,, Bachlani GN,, Yang XF,, Norgard MV . 2007. Evidence that RpoS (sigmaS) in Borrelia burgdorferi is controlled directly by RpoN (sigma54/sigmaN). J Bacteriol 189 : 21392144.[PubMed] [CrossRef]
53. Burtnick MN,, Downey JS,, Brett PJ,, Boylan JA,, Frye JG,, Hoover TR,, Gherardini FC . 2007. Insights into the complex regulation of rpoS in Borrelia burgdorferi . Mol Microbiol 65 : 277293.[PubMed] [CrossRef]
54. Xu H,, Caimano MJ,, Lin T,, He M,, Radolf JD,, Norris SJ,, Gherardini F,, Wolfe AJ,, Yang XF . 2010. Role of acetyl-phosphate in activation of the Rrp2-RpoN-RpoS pathway in Borrelia burgdorferi . PLoS Pathog 6 : e1001104. [PubMed] [CrossRef]
55. Lybecker MC,, Samuels DS . 2007. Temperature-induced regulation of RpoS by a small RNA in Borrelia burgdorferi . Mol Microbiol 64 : 10751089.[PubMed] [CrossRef]
56. Lybecker MC,, Abel CA,, Feig AL,, Samuels DS . 2010. Identification and function of the RNA chaperone Hfq in the Lyme disease spirochete Borrelia burgdorferi . Mol Microbiol 78 : 622635.[PubMed] [CrossRef]
57. Karna SL,, Sanjuan E,, Esteve-Gassent MD,, Miller CL,, Maruskova M,, Seshu J . 2011. CsrA modulates levels of lipoproteins and key regulators of gene expression critical for pathogenic mechanisms of Borrelia burgdorferi . Infect Immun 79 : 732744.[PubMed] [CrossRef]
58. Sze CW,, Li C . 2011. Inactivation of bb0184, which encodes carbon storage regulator A, represses the infectivity of Borrelia burgdorferi . Infect Immun 79 : 12701279.[PubMed] [CrossRef]
59. Ouyang Z,, Zhou J,, Norgard MV . 2014. CsrA (BB0184) is not involved in activation of the RpoN-RpoS regulatory pathway in Borrelia burgdorferi . Infect Immun 82 : 15111522.[PubMed] [CrossRef]
60. Miller CL,, Karna SL,, Seshu J . 2013. Borrelia host adaptation Regulator (BadR) regulates rpoS to modulate host adaptation and virulence factors in Borrelia burgdorferi . Mol Microbiol 88 : 105124.[PubMed] [CrossRef]
61. Boylan JA,, Posey JE,, Gherardini FC . 2003. Borrelia oxidative stress response regulator, BosR: a distinctive Zn-dependent transcriptional activator. Proc Natl Acad Sci U S A 100 : 1168411689.[PubMed] [CrossRef]
62. Katona LI,, Tokarz R,, Kuhlow CJ,, Benach J,, Benach JL . 2004. The fur homologue in Borrelia burgdorferi . J Bacteriol 186 : 64436456.[PubMed] [CrossRef]
63. Hyde JA,, Shaw DK,, Smith R III,, Trzeciakowski JP,, Skare JT . 2010. Characterization of a conditional bosR mutant in Borrelia burgdorferi . Infect Immun 78 : 265274.[PubMed] [CrossRef]
64. Samuels DS,, Radolf JD . 2009. Who is the BosR around here anyway? Mol Microbiol 74 : 12951299.[PubMed] [CrossRef]
65. Ouyang Z,, Kumar M,, Kariu T,, Haq S,, Goldberg M,, Pal U,, Norgard MV . 2009. BosR (BB0647) governs virulence expression in Borrelia burgdorferi . Mol Microbiol 74 : 13311343.[PubMed] [CrossRef]
66. Hyde JA,, Shaw DK,, Smith IR,, Trzeciakowski JP,, Skare JT . 2009. The BosR regulatory protein of Borrelia burgdorferi interfaces with the RpoS regulatory pathway and modulates both the oxidative stress response and pathogenic properties of the Lyme disease spirochete. Mol Microbiol 74 : 13441355.[PubMed] [CrossRef]
67. Ouyang Z,, Deka RK,, Norgard MV . 2011. BosR (BB0647) controls the RpoN-RpoS regulatory pathway and virulence expression in Borrelia burgdorferi by a novel DNA-binding mechanism. PLoS Pathog 7 : e1001272. [PubMed] [CrossRef]
68. Ouyang Z,, Zhou J,, Brautigam CA,, Deka R,, Norgard MV . 2014. Identification of a core sequence for the binding of BosR to the rpoS promoter region in Borrelia burgdorferi . Microbiology 160 : 851862.[PubMed] [CrossRef]
69. Wang P,, Dadhwal P,, Cheng Z,, Zianni MR,, Rikihisa Y,, Liang FT,, Li X . 2013. Borrelia burgdorferi oxidative stress regulator BosR directly represses lipoproteins primarily expressed in the tick during mammalian infection. Mol Microbiol 89 : 11401153.[PubMed] [CrossRef]
70. Troxell B,, Ye M,, Yang Y,, Carrasco SE,, Lou Y,, Yang XF . 2013. Manganese and zinc regulate virulence determinants in Borrelia burgdorferi . Infect Immun 81 : 27432752.[PubMed] [CrossRef]
71. Rogers EA,, Terekhova D,, Zhang HM,, Hovis KM,, Schwartz I,, Marconi RT . 2009. Rrp1, a cyclic-di-GMP-producing response regulator, is an important regulator of Borrelia burgdorferi core cellular functions. Mol Microbiol 71 : 15511573.[PubMed] [CrossRef]
72. Ryjenkov DA,, Tarutina M,, Moskvin OV,, Gomelsky M . 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol 187 : 17921798.[PubMed] [CrossRef]
73. Hengge R . 2009. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7 : 263273.[PubMed] [CrossRef]
74. Sondermann H,, Shikuma NJ,, Yildiz FH . 2012. You’ve come a long way: c-di-GMP signaling. Curr Opin Microbiol 15 : 140146.[PubMed] [CrossRef]
75. Novak EA,, Sultan SZ,, Motaleb MA . 2014. The cyclic-di-GMP signaling pathway in the Lyme disease spirochete, Borrelia burgdorferi. Front. Cell Infect Microbiol 4 : 56. [PubMed] [CrossRef]
76. Caimano MJ,, Kenedy MR,, Kairu T,, Desrosiers DC,, Harman M,, Dunham-Ems S,, Akins DR,, Pal U,, Radolf JD . 2011. The hybrid histidine kinase Hk1 is part of a two-component system that is essential for survival of Borrelia burgdorferi in feeding Ixodes scapularis ticks. Infect Immun 79 : 31173130.[PubMed] [CrossRef]
77. Freedman JC,, Rogers EA,, Kostick JL,, Zhang H,, Iyer R,, Schwartz I,, Marconi RT . 2010. Identification and molecular characterization of a cyclic-di-GMP effector protein, PlzA (BB0733): additional evidence for the existence of a functional cyclic-di-GMP regulatory network in the Lyme disease spirochete, Borrelia burgdorferi . FEMS Immunol Med Microbiol 58 : 285294.[PubMed] [CrossRef]
78. He M,, Ouyang Z,, Troxell B,, Xu H,, Moh A,, Piesman J,, Norgard MV,, Gomelsky M,, Yang XF . 2011. Cyclic di-GMP is essential for the survival of the Lyme disease spirochete in ticks. PLoS Pathog 7 : e1002133. [PubMed] [CrossRef]
79. Kostick JL,, Szkotnicki LT,, Rogers EA,, Bocci P,, Raffaelli N,, Marconi RT . 2011. The diguanylate cyclase, Rrp1, regulates critical steps in the enzootic cycle of the Lyme disease spirochetes. Mol Microbiol 81 : 219231.[PubMed] [CrossRef]
80. Groshong AM,, Blevins JS . 2014. Insights into the biology of Borrelia burgdorferi gained through the application of molecular genetics. Adv Appl Microbiol 86 : 41143.[PubMed] [CrossRef]
81. von Lackum K,, Stevenson B . 2005. Carbohydrate utilization by the Lyme borreliosis spirochete, Borrelia burgdorferi . FEMS Microbiol Lett 243 : 173179.[PubMed] [CrossRef]
82. Das R,, Hegyi H,, Gerstein M . 2000. Genome analyses of spirochetes: a study of the protein structures, functions and metabolic pathways in Treponema pallidum and Borrelia burgdorferi . J Mol Microbiol Biotechnol 2 : 387392.[PubMed]
83. Jain S,, Sutchu S,, Rosa PA,, Byram R,, Jewett MW . 2012. Borrelia burgdorferi harbors a transport system essential for purine salvage and mammalian infection. Infect Immun 80 : 30863093.[PubMed] [CrossRef]
84. Ouyang Z,, He M,, Oman T,, Yang XF,, Norgard MV . 2009. A manganese transporter, BB0219 (BmtA), is required for virulence by the Lyme disease spirochete, Borrelia burgdorferi . Proc Natl Acad Sci U S A 106 : 34493454.[PubMed] [CrossRef]
85. Hoon-Hanks LL,, Morton EA,, Lybecker MC,, Battisti JM,, Samuels DS,, Drecktrah D . 2012. Borrelia burgdorferi malQ mutants utilize disaccharides and traverse the enzootic cycle. FEMS Immunol Med Microbiol 66 : 157165.[PubMed] [CrossRef]
86. Deng Z,, Roberts D,, Wang X,, Kemp RG . 1999. Expression, characterization, and crystallization of the pyrophosphate-dependent phosphofructo-1-kinase of Borrelia burgdorferi . Arch Biochem Biophys 371 : 326331.[PubMed] [CrossRef]
87. Moore SA,, Ronimus RS,, Roberson RS,, Morgan HW . 2002. The structure of a pyrophosphate-dependent phosphofructokinase from the Lyme disease spirochete Borrelia burgdorferi . Structure 10 : 659671.[PubMed] [CrossRef]
88. Gebbia JA,, Backenson PB,, Coleman JL,, Anda P,, Benach JL . 1997. Glycolytic enzyme operon of Borrelia burgdorferi: characterization and evolutionary implications. Gene 188 : 221228.[PubMed] [CrossRef]
89. Barbour AG . 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57 : 521525.[PubMed]
90. Tilly K,, Elias AF,, Errett J,, Fischer E,, Iyer R,, Schwartz I,, Bono JL,, Rosa P . 2001. Genetics and regulation of chitobiose utilization in Borrelia burgdorferi . J Bacteriol 183 : 55445553.[PubMed] [CrossRef]
91. Hackman RH . 1982. Structure and function in tick cuticle. Annu Rev Entomol 27 : 7595.[PubMed] [CrossRef]
92. Rhodes RG,, Atoyan JA,, Nelson DR . 2010. The chitobiose transporter, chbC, is required for chitin utilization in Borrelia burgdorferi . BMC Microbiol 10 : 21. [PubMed] [CrossRef]
93. Barabote RD,, Saier MH Jr . 2005. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69 : 608634.[PubMed] [CrossRef]
94. Clore GM,, Venditti V . 2013. Structure, dynamics and biophysics of the cytoplasmic protein-protein complexes of the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Trends Biochem Sci 38 : 515530.[PubMed] [CrossRef]
95. Gorke B,, Stulke J . 2008. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6 : 613624.[PubMed] [CrossRef]
96. Godany A,, Vidova B,, Janecek S . 2008. The unique glycoside hydrolase family 77 amylomaltase from Borrelia burgdorferi with only catalytic triad conserved. FEMS Microbiol Lett 284 : 8491.[PubMed] [CrossRef]
97. Jahreis K,, Pimentel-Schmitt EF,, Bruckner R,, Titgemeyer F . 2008. Ins and outs of glucose transport systems in eubacteria. FEMS Microbiol Rev 32 : 891907.[PubMed] [CrossRef]
98. Ostberg Y,, Berg S,, Comstedt P,, Wieslander A,, Bergstrom S . 2007. Functional analysis of a lipid galactosyltransferase synthesizing the major envelope lipid in the Lyme disease spirochete Borrelia burgdorferi . FEMS Microbiol Lett 272 : 2229.[PubMed] [CrossRef]
99. Jensen MO,, Park S,, Tajkhorshid E,, Schulten K . 2002. Energetics of glycerol conduction through aquaglyceroporin GlpF. Proc Natl Acad Sci U S A 99 : 67316736.[PubMed] [CrossRef]
100. Chen LY . 2013. Glycerol modulates water permeation through Escherichia coli aquaglyceroporin GlpF. Biochim Biophy Acta 1828 : 17861793.[PubMed] [CrossRef]
101. Foster JW,, Moat AG . 1980. Nicotinamide adenine dinucleotide biosynthesis and pyridine nucleotide cycle metabolism in microbial systems. Microbiol Rev 44 : 83105.[PubMed]
102. Gazzaniga F,, Stebbins R,, Chang SZ,, McPeek MA,, Brenner C . 2009. Microbial NAD metabolism: lessons from comparative genomics. Microbiol Mol Biol Rev 73 : 529541.[PubMed] [CrossRef]
103. Wolfe AJ . 2005. The acetate switch. Microbiol Mol Biol Rev 69 : 1250.[PubMed] [CrossRef]
104. Boylan JA,, Hummel CS,, Benoit S,, Garcia-Lara J,, Treglown-Downey J,, Crane EJ III,, Gherardini FC . 2006. Borrelia burgdorferi bb0728 encodes a coenzyme A disulphide reductase whose function suggests a role in intracellular redox and the oxidative stress response. Mol Microbiol 59 : 475486.[PubMed] [CrossRef]
105. Eggers CH,, Caimano MJ,, Malizia RA,, Kariu T,, Cusack B,, Desrosiers DC,, Hazlett KR,, Claiborne A,, Pal U,, Radolf JD . 2011. The coenzyme A disulphide reductase of Borrelia burgdorferi is important for rapid growth throughout the enzootic cycle and essential for infection of the mammalian host. Mol Microbiol 82 : 679697.[PubMed] [CrossRef]
106. Gazanion E,, Garcia D,, Silvestre R,, Gerard C,, Guichou JF,, Labesse G,, Seveno M,, Cordeiro-Da-Silva A,, Ouaissi A,, Sereno D,, Vergnes B . 2011. The Leishmania nicotinamidase is essential for NAD+ production and parasite proliferation. Mol Microbiol 82 : 2138.[PubMed] [CrossRef]
107. Skare JT,, Carroll JA,, Yang XF,, Samuels DS,, Akins DR, . 2010. Gene Regulation, Transcriptomics and Proteomics, p 67101. In Samuels DS,, Radolf JD (ed.), Borrelia: Molecular Biology, Host Interaction and Pathogenesis. Caister Academic Press, Norfolk, UK.
108. Lee RJ,, Baust JG . 1987. Cold-hardiness in the Antartic tick, Ixodes uriae Physiol. Zool 60 : 499506.
109. Vandyk JK,, Bartholomew DM,, Rowley WA,, Platt KB . 1996. Survival of Ixodes scapularis (Acari: Ixodidae) exposed to cold. J Med Entomol 33 : 610.[PubMed] [CrossRef]
110. Ojaimi C,, Brooks C,, Casjens S,, Rosa P,, Elias A,, Barbour A,, Jasinskas A,, Benach J,, Katona L,, Radolf J,, Caimano M,, Skare J,, Swingle K,, Akins D,, Schwartz I . 2003. Profiling of temperature-induced changes in Borrelia burgdorferi gene expression by using whole genome arrays. Infect Immun 71 : 16891705.[PubMed] [CrossRef]
111. Rhodes RG,, Coy W,, Nelson DR . 2009. Chitobiose utilization in Borrelia burgdorferi is dually regulated by RpoD and RpoS. BMC Microbiol 9 : 108. [PubMed] [CrossRef]
112. Sze CW,, Smith A,, Choi YH,, Yang X,, Pal U,, Yu A,, Li C . 2013. Study of the response regulator Rrp1 reveals its regulatory role in chitobiose utilization and virulence of Borrelia burgdorferi . Infect Immun 81 : 17751787.[PubMed] [CrossRef]
113. Hyde JA,, Seshu J,, Skare JT . 2006. Transcriptional profiling of Borrelia burgdorferi containing a unique bosR allele identifies a putative oxidative stress regulon. Microbiology 152 : 25992609.[PubMed] [CrossRef]
114. Deutscher J . 2008. The mechanisms of carbon catabolite repression in bacteria. Curr Opin Microbiol 11 : 8793.[PubMed] [CrossRef]
115. Maeda N,, Funahashi T,, Hibuse T,, Nagasawa A,, Kishida K,, Kuriyama H,, Nakamura T,, Kihara S,, Shimomura I,, Matsuzawa Y . 2004. Adaptation to fasting by glycerol transport through aquaporin 7 in adipose tissue. Proc Natl Acad Sci U S A 101 : 1780117806.[PubMed] [CrossRef]
116. Moat AG,, Foster JW,, Spector MP . 2002. Microbial Physiology, 4th ed. Wiley-Liss, New York. [CrossRef]
117. Roberson RS,, Ronimus RS,, Gephard S,, Morgan HW . 2001. Biochemical characterization of an active pyrophosphate-dependent phosphofructokinase from Treponema pallidum . FEMS Microbiol Lett 194 : 257260.[PubMed] [CrossRef]
118. Saier MH Jr,, Eng BH,, Fard S,, Garg J,, Haggerty DA,, Hutchinson WJ,, Jack DL,, Lai EC,, Liu HJ,, Nusinew DP,, Omar AM,, Pao SS,, Paulsen IT,, Quan JA,, Sliwinski M,, Tseng TT,, Wachi S,, Young GB . 1999. Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim Biophys Acta 1422 : 156.[PubMed] [CrossRef]
119. Deutscher J,, Ake FM,, Derkaoui M,, Zebre AC,, Cao TN,, Bouraoui H,, Kentache T,, Mokhtari A,, Milohanic E,, Joyet P . 2014. The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol Mol Biol Rev 78 : 231256.[PubMed] [CrossRef]
120. Lengeler JW,, Jahreis K . 2009. Bacterial PEP-dependent carbohydrate: phosphotransferase systems couple sensing and global control mechanisms. Contrib Microbiol 16 : 6587.[PubMed] [CrossRef]
121. Hogema BM,, Arents JC,, Bader R,, Eijkemans K,, Yoshida H,, Takahashi H,, Aiba H,, Postma PW . 1998. Inducer exclusion in Escherichia coli by non-PTS substrates: the role of the PEP to pyruvate ratio in determining the phosphorylation state of enzyme IIAGlc. Mol Microbiol 30 : 487498.[PubMed] [CrossRef]


Generic image for table

genes encoding proteins involved in carbohydrate metabolism

Citation: Corona A, Schwartz I. 2015. : Carbon Metabolism and the Tick-Mammal Enzootic Cycle, p 167-184. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0011-2014

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