Spirochaetes

Abstract

Species in the phylum Spirochaetes (order: Spirochaetales) are thin, spiral‐shaped or wave‐like, highly motile bacteria that are best visualised by darkfield microscopy. Spirochaetes are Gram‐negative‐like, in that they possess inner and outer membranes separated by a peptidoglycan‐containing periplasmic space. Beyond these ultrastructural similarities, few parallels exist with conventional Gram‐negative bacteria. There have been more than 90 spirochaete species identified, including the well‐known pathogenic, disease‐causing species Treponema pallidum (syphilis), Leptospira sp. (leptospirosis) and Borrelia burgdorferi (Lyme disease). The phylogenetic relationship among spirochaetes is evident at the level of gross phenotypic characteristics, which include a distinctive morphology derived from the presence of periplasmic flagella. In this article, the authors describe the genomic, physiologic, structural and functional features that make Spirochaetes unique among the prokaryotes.

Key Concepts:

  • Spirochaetes are a genetically and morphologically distinct group of bacteria.

  • Spirochaetes are thin spiral‐shaped or wave‐like bacteria that are highly motile.

  • Endoflagella/periplasmic flagella provide spirochaetes with their characteristic corkscrew‐like motility.

  • Spirochaetes differ from typical Gram‐negative bacteria at the ultrastructural level.

  • Spirochaetes are chemo‐organotrophic, grow in diverse conditions and are comprised of both pathogenic and nonpathogenic members.

  • Complete genome sequencing has allowed for the characterisation and differentiation of spirochaetes at the genetic level.

  • Medically important spirochaetes belong to the three genera Borrelia, Leptospira and Treponema.

Keywords: periplasmic endoflagella; syphilis; leptospirosis; Lyme disease; Treponema; Leptospira; Borrelia

Figure 1.

Evolutionary relationships among representatives of Spirochaetales. The evolutionary history was inferred using the Neighbor‐Joining method. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) is shown next to the branches (Felsenstein, ). The tree is drawn to scale, with branch lengths computed using the p‐distance method (Nei and Kumar, ). The analysis involved 37 nucleotide sequences. All ambiguous positions were removed for each sequence pair. There were a total of 1492 positions in the final dataset. Evolutionary analyses were conducted in MEGA5 Tamura et al. ().

Figure 2.

Schematic diagram of the three representative genera Treponema (top image), Leptospira (middle image), and Borrelia (bottom image).

Figure 3.

Treponema pallidum has a flat‐wave morphology. Representative micrographs show the flat‐wave morphology of T. pallidum as revealed by darkfield microscopy (a and b) and by epifluorescence microscopy (c and d). Panels c and d show sequential images of the same treponeme; note how the leftward segment changes from helical to linear as it moves away from the focal plane. Panels e and f show darkfield images of Borrelia burgdorferi in two different orientations. Arrows and asterisks indicate regions of the spirochaetes that are parallel to the z axis or in the xy plane, respectively. Reproduced with permission of Izard et al. (). © American Society for Microbiology.

Figure 4.

The T. pallidum cell envelope architecture. The space between the outer and cytoplasmic membranes increases from approximately 23 nm to approximately 49 nm in regions containing the periplasmic flagella (a and c). The periplasmic flagella (blue line) remain closely associated with the cell cylinder following removal of the outer membrane through repeated centrifugation (b and d). The 4 nm lipid bilayer composition of the cytoplasmic membrane is visible in higher magnification views (e and g). The locations of the cytoplasmic filaments (red line), lipoprotein layer (purple circles) and peptidoglycan (orange line) are indicated (e). a, b and e are longitudinal views, while c and d are the cross‐section views. Most membrane proteins (coloured in orange) are anchored to the cytoplasmic membrane (CM) just underneath the thin layer of peptidoglycan (PG). A model of the T. pallidum cell envelope is shown in (f). Rare outer membrane proteins (coloured in purple) are exposed on the outer membrane (OM). Reproduced with permission from Liu et al. (). © Elsevier.

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References

Angelov A, Liebl S, Ballschmiter M et al. (2010) Genome sequence of the polysaccharide‐degrading, thermophilic anaerobe Spirochaeta thermophila DSM 6192. Journal of Bacteriology 192: 6492–6493.

Bharti AR, Nally JE, Ricaldi JN et al. (2003) Leptospirosis: a zoonotic disease of global importance. Lancet Infectious Disease 3: 757–771.

Bulach DM, Zuerner RL, Wilson P et al. (2006) Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proceedings of the National Academy of Sciences of the USA 103: 14560–14565.

Calderaro A, Gorrini C, Piccolo G et al. (2014) Identification of Borrelia species after creation of an in‐house MALDI‐TOF MS database. PLoS One 9: e88895.

Casjens S, Palmer N, vanVugt R et al. (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. Molecular Microbiology 35: 490–516.

Casjens SR, Mongodin EF, Qiu WG et al. (2011) Whole‐genome sequences of two Borrelia afzelii and two Borrelia garinii Lyme disease agent isolates. Journal of Bacteriology 193: 6995–6996.

Casjens SR, Mongodin EF, Qiu WG et al. (2012) Genome stability of Lyme disease spirochetes: comparative genomics of Borrelia burgdorferi plasmids. PLoS One 7: e33280.

Čejková D, Zobaníková M, Chen L et al. (2012) Whole genome sequences of three Treponema pallidum ssp. pertenue strains: yaws and syphilis treponemes differ in less than 0.2% of the genome sequence. PLOS Neglected Tropical Diseases 6: e1471.

Chan EC and McLaughlin R (2000) Taxonomy and virulence of oral spirochetes. Oral Microbiology and Immunology 15: 1–9.

Charon NW, Cockburn A, Li C et al. (2012) The unique paradigm of spirochete motility and chemotaxis. Annual Review of Microbiology 66: 349–370.

Embers M (ed.) (2013) The Pathogenic Spirochetes: Strategies for Evasion of Host Immunity and Persistence. New York, NY: Springer.

Eshghi A, Lourdault K, Murray GL et al. (2012) Leptospira interrogans catalase is required for resistance to H2O2 and for virulence. Infection and Immunity 80: 3892–3899.

Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

Fraser CM, Casjens S, Huang WM et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580–586.

Fraser CM, Norris SJ, Weinstock GM et al. (1998) Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281: 375–388.

Giacani L and Lukehart SA (2014) The endemic treponematoses. Clinical Microbiology Reviews 27: 89–115.

Glockner G, Lehmann R, Romualdi A et al. (2004) Comparative analysis of the Borrelia garinii genome. Nucleic Acids Research 32: 6038–6046.

Gupta RS, Mahmood S and Adeolu M (2013) A phylogenomic and molecular signature based approach for characterization of the phylum Spirochaetes and its major clades: proposal for a taxonomic revision of the phylum. Frontiers in Microbiology. 4:217.

Houhamdi L and Raoult D (2005) Excretion of living Borrelia recurrentis in feces of infected human body lice. Journal of Infectious Diseases 191: 1898–1906.

Ivanova LB, Tomova A, Gonzalez‐Acuna D et al. (2013) Borrelia chilensis, a new member of the Borrelia burgdorferi sensu lato complex that extends the range of this genospecies in the Southern Hemisphere. Environmental Microbiology. doi:10.1111/1462‐2920.12310.

Izard J, Renken C, Hsieh CE et al. (2009) Cryo‐electron tomography elucidates the molecular architecture of Treponema pallidum, the syphilis spirochete. Journal of Bacteriology 191: 7566–7580.

Kuehn BM (2013) CDC estimates 300 000 US cases of Lyme disease annually. Journal of the American Medical Association 310: 1110.

Larsson C, Andersson M, Pelkonen J et al. (2006) Persistent brain infection and disease reactivation in relapsing fever borreliosis. Microbes and Infection 8: 2213–2219.

Lescot M, Audic S, Robert C et al. (2008) The genome of Borrelia recurrentis, the agent of deadly louse‐borne relapsing fever, is a degraded subset of tick‐borne Borrelia duttonii. PLOS Genetics 4: e1000185.

Liu J, Howell JK, Bradley SD et al. (2010) Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography. Journal of Molecular Biology 403: 546–561.

Liu J, Lin T, Botkin DJ et al. (2009) Intact flagellar motor of Borrelia burgdorferi revealed by cryo‐electron tomography: evidence for stator ring curvature and rotor/c‐ring assembly flexion. Journal of Bacteriology 191: 5026–5036.

Ludwig W, Euzéby J and Whitman WB (2010) Road map of the phyla Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. In: Parte AC (ed.) Bergey's Manual of Systematic Bacteriology, vol. 4, pp. 1–17. New York, NY: Springer.

Malmström J, Beck M, Schmidt A et al. (2009) Proteome‐wide cellular protein concentrations of the human pathogen Leptospira interrogans. Nature 460: 762–765.

Murray GL, Srikram A, Henry R et al. (2010) Mutations affecting Leptospira interrogans lipopolysaccharide attenuate virulence. Molecular Microbiology 78: 701–709.

Nascimento AL, Ko AI, Martins EA et al. (2004) Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. Journal of Bacteriology 186: 2164–2172.

Nei M and Kumar S (2000) Molecular Evolution and Phylogenetics. New York, NY: Oxford University Press.

Newman L, Kamb M, Hawkes S et al. (2013) Global estimates of syphilis in pregnancy and associated adverse outcomes: analysis of multinational antenatal surveillance data. PLoS Medicine 10: e1001396.

Paster BJ (2011) Phylum XV. Spirochaetes Garrity and Holt 2001. In: Krieg NR, Ludwig W, Whitman WB et al. (eds) Bergey's Manual of Systematic Bacteriology, vol. 4, pp. 471–566. New York, NY: Springer Publishing Company.

Pětrošová H, Pospíšilová P, Strouhal M et al. (2013) Resequencing of Treponema pallidum ssp. pallidum strains Nichols and SS14: correction of sequencing errors resulted in increased separation of syphilis treponeme subclusters. PLoS One 8: e74319.

Pětrošová H, Zobaníková M, Čejková D et al. (2012) Whole genome sequence of Treponema pallidum ssp. pallidum, strain Mexico A, suggests recombination between yaws and syphilis strains. PLOS Neglected Tropical Diseases 6: e1832.

Picardeau M (2013) Diagnosis and epidemiology of leptospirosis. Médecine et Maladies Infectieuses 43: 1–9.

Picardeau M, Bulach DM, Bouchier C et al. (2008) Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis. PLoS One 3: e1607.

Platonov AE, Karan LS, Kolyasnikova NM et al. (2011) Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerging Infectious Diseases 17: 1816–1823.

Ren SX, Fu G, Jiang XG et al. (2003) Unique physiological and pathogenic features of Leptospira interrogans revealed by whole‐genome sequencing. Nature 422: 888–893.

Ristow P, Bourhy P, da Cruz McBride FW et al. (2007) The OmpA‐like protein Loa22 is essential for leptospiral virulence. PLoS Pathogens 3: e97.

Ritalahti KM, Justicia‐Leon SD, Cusick KD et al. (2012) Sphaerochaeta globosa gen. nov., sp. nov. and Sphaerochaeta pleomorpha sp. nov., free‐living, spherical spirochaetes. International Journal of Systematic and Evolutionary Microbiology. 62: 210–216.

Rudenko N, Golovchenko M, Grubhoffer L and Oliver JH (2011) Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks and Tick‐Borne Diseases 2: 123–128.

Schutzer SE, Fraser‐Liggett CM, Casjens SR et al. (2011) Whole‐genome sequences of thirteen isolates of Borrelia burgdorferi. Journal of Bacteriology 193: 1018–1020.

Seshadri R, Myers GS, Tettelin H et al. (2004) Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proceedings of the National Academy of Sciences of the USA 101: 5646–5651.

Šmajs D, Norris SJ and Weinstock GM (2012) Genetic diversity in Treponema pallidum: implications for pathogenesis, evolution and molecular diagnostics of syphilis and yaws. Infection, Genetics and Evolution 12: 191–202.

Šmajs D, Zobaníková M, Strouhal M et al. (2011) Complete genome sequence of Treponema paraluiscuniculi, strain Cuniculi A: the loss of infectivity to humans is associated with genome decay. PLoS One 6: e20415.

Tamura K, Peterson D, Peterson N et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.

Visser MB and Ellen RP (2011) New insights into the emerging role of oral spirochetes in periodontal disease. Clinical Microbiology and Infection 17: 502–512.

Walker EM, Zampighi GA, Blanco DR, Miller JN and Lovett MA (1989) Demonstration of rare protein in the outer membrane of Treponema pallidum subsp. pallidum by freeze‐fracture analysis. Journal of Bacteriology 171: 5005–5011.

Wang G, van Dam AP, Schwartz I and Dankert J (1999) Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clinical Microbiology Reviews 12: 633–653.

Further Reading

Adler B, Lo M, Seemann T and Murrray GL (2011) Pathogenesis of leptospirosis: the influence of genomics. Veterinary Microbiology 153: 73–81.

Adler B and de la Pena MA (2010) Leptospira and leptospirosis. Veterinary Microbiology 140: 287–296.

Brisson D, Drecktrah D, Eggers CH and Samuels DS (2012) Genetics of Borrelia burgdorferi. Annual Review of Genetics 46: 515–536.

Frederick JR, Sarkar J, McDowell JV and Marconi RT (2011) Molecular signaling mechanisms of the periopathogen, Treponema denticola. Journal of Dental Research 90: 1155–1163.

Ho EL and Lukehart SA (2011) Syphilis: using modern approaches to understand an old disease. Journal of Clinical Investigation 121: 4584–4592.

LaFond RE and Lukehart SA (2006) Biological basis for syphilis. Clinical Microbiology Reviews 19: 29–49.

Radolf JD, Caimano MJ, Stevenson B and Hu LT (2012) Of ticks, mice and men: understanding the dual‐host lifestyle of Lyme disease spirochaetes. Nature Reviews Microbiology 10: 87–99.

Samuels DS and Radolf JD (eds) (2010) Borrelia: Molecular Biology, Host Interaction and Pathogenesis. Norfolk: Caister Academic Press.

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Houston, Simon, Taylor, John S, and Cameron, Caroline E(Jul 2014) Spirochaetes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000466.pub3]