Borrelia mayonii

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1. Classification

Higher order taxa

Domain = Bacteria; Phylum = Spirochaetes; Class = Spirochaetia; Order = Spirochaetales; Family = Spirochaetaceae; Genus = Borrelia

Species

Borrelia mayonii

2. Description and significance

Borrelia mayonii is a genospecies of Borrelia burgdorferi sensu lato which has been recently discovered by the Mayo Clinic. B. burgdorferi sensu lato is responsible for causing Lyme borreliosis disease, which is a prevalent tick-borne disease found in the northern hemisphere (1). Although B. mayonii is transmitted through the same vector as other Borrelia strains (2), Ixodes scapularis, commonly known as the blacklegged tick, the genospecies has novel characteristics and symptoms that fall outside the range of characteristics and symptoms normally checked by clinicians. The Mayo Clinic first noticed B. mayonii after six out of 100,545 clinical specimens sent for routine PCR came back atypical for the oppA1 gene used to detect the presence of B. burgdorferi sensu lato (1). It is notably distinct from other B. burgdorferi sensu lato genospecies that cause Lyme disease because of the substantially elevated levels of spirochetemia in acutely ill patients (1). Current research is still establishing the basic characteristics of this new genospecies.

According to the Mayo Clinic, Lyme borreliosis is the most common tick-borne disease in the northern hemisphere (1). The disease’s high prevalence warrants attention from both the general population and clinicians so infections can be recognized and treated quickly and efficiently. In order to do this, it is important to understand the pathogens which cause the disease. B. mayonii infects hosts and produces symptoms different than other B. burgdoferi sensu lato genospecies, which creates the risk of overlooking infected individuals who do not fit the stereotypical presentation of Lyme disease (1). Therefore, it is important to characterize and raise awareness of this new genospecies and the way it is transmitted and infects. Furthermore, the recent discovery of a new B. burgdoferi sensu lato genospecies raises the question: are there other new genospecies that have recently evolved?

3. Genome structure

The B. mayonii genome is approximately 1.31 Mbp in size and comprised of a linear chromosome with an additional eight linear and seven circular plasmids. The linear chromosome shares 93.83% average nucleotide identity (ANI) with other genospecies, consistent with its designation as a new Borrelia burgdorferi sensu lato (Bbsl) genospecies (3). This main chromosome is highly conserved, with low sequence variation across the entire length. The extrachromosomal plasmids on the other hand are structurally and genetically variable, encoding for proteins necessary for infecting tick hosts, pathogenicity, and immune cell invasion (3). The linear and circular plasmids range in size from 5 to 56 kbp with an average GC content of 26.7%. One linear plasmid in particular, Ip25, shares overall gene organization with plasmids from B. burgdorferi and has been identified in other Bbsl genospecies as necessary for infection (4). The lower coding density of plasmids and high pseudogenes among Bbsl genospecies are believed to be the source of divergence and adaptation to different host species and will require more research into the species’ mechanisms of host infection (4).

4. Cell structure

The Borrelia species denotes a sensu lato complex of motile spirochetes that presents in human hosts as a localized infection prior to dispersal to the nervous system and other organs (1). Like B. burgdorferi, B. mayonii is characterized by a helical-shaped bacterium with an inner and outer membrane. It lacks lipopolysaccharides and contains immunoreactive glycolipids in its place. The periplasm space between the two membranes contains the cell’s flagella, which interacts with the cell cylinder to drive cellular motion. This force is particularly important in host infection to travel through host tissue. The B. burgdorferi sensu lato is pleomorphic, changing its morphology in response to the environment and has the ability to form biofilms (5).

Due to the genospecies status as a recently discovered species, more research must be conducted in order to elucidate cellular characteristics that distinguish it from the rest of the sensu lato complex. One particular interest is in the substantially high spirochaetaemia count that differentiates B. mayonii infected patients from the low count in B. burgdorferi patients and possible cellular structures that underlie it.

5. Metabolic processes

B. burgdoferi spirochetes, including B. mayonii, exist in an arthropod vector-vertebrate reservoir host transmission chain and thus have very limited metabolic capacity, instead relying on the host for survival (6). The B. burgdoferi spirochetes lack de novo biosynthesis pathways for nucleotides, amino acids, fatty acids, and coenzyme factors (6). Metabolic intermediates are obtained through blood meal when residing in the tick vector, though the exact metabolism processes within the tick are largely unknown (6). Purines, amino acids, and carbohydrates are taken up by the spirochetes from these blood meals (6).

Hoxmeier et al have studied the metabolic differences between B. burgdoferi and B. mayonii in I. scapularis. They found differences in the tick’s purine and amino acid metabolism as the pathogen uptakes the compounds from the blood meal (6). The study specifically notes that B. mayonii metabolics differs from B. burgdoferi metabolics more drastically in later stages of infection (6). B. mayonii was shown to utilize more galactose, which may be important in the development of the spirochetes in the tick vector, than B. burgdoferi (6). Glucose and maltose are also utilized differently between B. mayonii and B. burgdoferi (6). After four days of feeding on blood, ticks infected with B. mayonii showed sharp declines in the amounts of cholesterol, ethanolamine, ethanolamine phosphate, and glycerol-3-phosphate whereas ticks infected with B. burgdoferi did not show this pattern (6). More research is needed to determine if the metabolic differences are attributed to the higher number of spirochetes observed with B. mayonii or if it is truly a difference in metabolic capability.

6. Ecology

B. mayonii was discovered by the Mayo Clinic after DNA sequencing and analysis of I. scapularis ticks collected from Barron County, Wisconsin, following two cases of potential patient exposure (1). Thus far, B. mayonii is only associated with the upper Midwestern United States, in contrast to B. burgdorferi in the eastern United States. Borrelia strains tend to demonstrate regional difference, but evidence suggests that the vector efficiency of the blacklegged tick does not vary by region. If the vector efficiency does not depend on region, then another unknown factor is at play for the regional isolation of B. mayonii in the Midwest (2). Mice, the suspected rodent involved with B. mayonii transmission, presented Borrelia spirochetes in the bladder tissue, heart tissue, and spinal cord after euthanasia, which demonstrates how B. mayonii spreads during host infection (7).

7. Pathology

Due to the recent discovery of B. mayonii, the pathogenic potential of this particular Borrelia strain has yet to be established (8). B. mayonii shares a vector with other known pathogenic species, which adds to the complication in assessing pathogenic potential because of the possibility for mixed infections. However, B. mayonii has drawn attention to itself for perhaps being a more virulent member of the genus Borreliae. The evidence found since its discovery suggests that it produces more spirochetes in the blood than its counterparts (8).

Transmission/Hosts

B. mayonii was detected from a host-seeking blacklegged tick, I. scapularis, which is the primary vector of B. burgdorferi in the eastern United States (2). Further evidence suggests that host-seeking I. scapularis is a competent vector for B. mayonii, both in a laboratory and field setting, and that I. scapularis nymphs are the most likely primary vectors of B. mayonii, similar to B. burgdorferi (2). Natural vertebrate reservoirs are still unknown for B. mayonii, but current research suggests that the same rodent species involved in transmission for B. burgdorferi, M. musculus, should be suspected for primary transmission of B. mayonii. Transmission for B. mayonii is also suspected to be enzootic, like B. burgdorferi (2).

Infection Rate

Lyme borreliosis, the primary tick-borne disease caused by some Borrelia species, including B. mayonii, affects an estimated 300,000 people in the US per year, and is the most common tick-borne disease in the United States (1). The blacklegged tick is the most likely primary vector for human infection with Lyme borreliosis. B. mayonii was discovered to have infection rates of 4% in nymphs and 5% in adults after collection in 2014, which is lower than infection rates for the well-known strain, B. burgdorferi (2). Infected mice also produced infected I. scapularis nymphs, with infection rates ranging from 2.5-25.0% (2). There is no evidence of infection within 24 or 48 hours of I. scapularis attachment. After 72 hours, the probability of transmission was 31%, and after 72 hours, the probability was 57%. These transmission rates from a single I. scapularis nymph are comparable to those of B. burgdorferi (9).

Symptoms of Infection

The presence of B. mayonii in humans has only been documented six times, and no definitive pattern of symptoms was clear (1). The Mayo Clinic reported five of the infected patients having fever, four with a diffuse or local rash, three with symptoms suggestive of neurological inclusion, and one with knee pain and swelling (1). Two of the six patients were admitted to the hospital (1). Other documented symptoms included headache, neck pain, fatigue, myalgia, and nausea or vomiting (1). Fever and nausea or vomiting are not characteristic symptoms of B. burgdoferi, which reinforces the need for distinction of the novel genospecies B. mayonii (1).

7. Key microorganisms

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8. Current Research

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9. References

1. B.S. Pritt, P.S. Mead, D.K Hoang Johnson, D.F. Neitzel, L.B. Respicio-Kingry, J.P. Davis, E. Schiffman, L.M. Sloan, M.E. Schriefer, A.J. Replogle, S.M. Paskewtiz, J.A. Ray, J. Bjork, C.R. Steward, A. Deedon, X. Lee, L.C. Kingry, T.K. Miller, M.A. Feist, E.S. Theel, R. Patel, C.L. Irish, J.M. Petersen. 2016. Identification of a novel pathogenic Borrelia species causing Lyme borreliosis with unusually high spirochaetaemia: a descriptive study. The Lancet Infectious Diseases 16:556-64

2. M.C. Dolan, A. Hojgaard, J.C. Hoxmeier, A.J. Replogle, L.B. Respicio-Kingry, C. Sexton, M.A Williams, B.S. Pritt, M.E. Schriefer, L. Eisen. 2016. Vector competence of the blacklegged tick, Ixodes scapularis, for the recently recognized Lyme borreliosis spirochete Candidatus Borrelia mayonii. Ticks and Tick-borne Diseases 7:665-669.

3. Kingry LC, Batra D, Replogle A, Rowe LA, Pritt BS, Petersen JM (2016) Whole Genome Sequence and Comparative Genomics of the Novel Lyme Borreliosis Causing Pathogen, Borrelia mayonii. PLoS ONE 11(12): e0168994. doi:10.1371/journal.pone.0168994

4. Fraser, CM., Casjens, S., Huang, WM., Sutton, GG., Clayton, R. et al. "Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi." Nature. 1997 Dec 11;390(6660):580-6

5. Meriläinen, L., Herranen, A., Schwarzbach, A., & Gilbert, L. (2015). Morphological and biochemical features of Borrelia burgdorferi pleomorphic forms. Microbiology, 161(Pt 3), 516–527.

6. Hoxmeier, J. C., Fleshman, A. C., Broeckling, C. D., Prenni, J. E., Dolan, M. C., Gage, K. L., & Eisen, L. 2017. Metabolomics of the tick-Borrelia interaction during the nymphal tick blood meal. Scientific Reports, 7, 44394.

7. M.C. Dolan, N.E. Breuner, A. Hojgaard, J.C. Hoxmeier, M.A. Pilgard, A.J. Replogle, L. Eisen. 2017. Duration of Borrelia mayonii infectivity in an experimental mouse model for feeding Ixodes scapularis larvae. Ticks and Tick-Borne Diseases 8(1):196-200.

8. S. J. Cutler, E. Ruzic-Sabljic, A. Potkonjak. 2017. Emerging borreliae – Expanding beyond Lyme borreliosis. Molecular and Cellular Probes 31: 22-27.

9. M.C. Dolan, N.E. Breuner, A. Hojgaard, K.A. Boegler, J.C. Hoxmeier, A.J. Replogle, L. Eisen. 2017. Transmission of the Lyme Disease Spirochete Borrelia mayonii in Relation to Duration of Attachment by Nymphal Ixodes scapularis. Journal of Medical Entomology 54(5): 1360-1364.

10. P. H. Boyer, S. J. De Martino, Y. Hansmann, L. Zilliox, N. Boulanger, B. Jaulhac. 2017. No evidence of Borrelia mayonii in an endemic area for Lyme borreliosis in France. Parasites and Vectors 10:282.