GENOMOSYSTEMATICS OF RICKETTSIAE

Cover Page


Cite item

Full Text

Abstract

The definition of the term genome was given by the German botanist G. Winkler almost one hundred years ago in 1920. A genome  definition for bacterial (rickettsia) with a single chromosome was  recently presented from the perspective of information theory,  biology and bioinformatics as the information chain of nucleotides.  The systematics of rickettsiae (obligate intracellular microorganisms) is based on a limited number of phenotypic characters.  Classifications built on the analysis of genes, fragments of genomes  and their concatenations cause discussion. Application of the Formal  Order Analysis (FOA, http://foarlab.org) in the study of complete  genomes allowed to submit the systematics of representatives of the family Rickettsiaceae. This approach confirmed the existence of  typhus group (TG), spotted fever group (SFG), and an «ancestral»  group within the genus Rickettsia, and allowed the isolation of the  Rickettsia felis group within this genus, located between the  «ancestral» group and the SFG and the R. akari group on the border  between the SFG group and the genus Orientia. The development of  the tools of FOA — «Map of Genes» and «Matrix of Similarity» —  helped to conduct an in-depth study of the complete genomes of  rickettsia, taking into account the characteristics of their genes and  noncoding sequences. Application of these instruments, with the  help of the obtained classification, confirmed the notion of ecological  features of rickettsia, the structure of nosological forms and the  epidemiological patterns of rickettsiosis, and made it possible to  assess the virulence of the strains of the two most pathogenic  species of rickettsia, R. prowazekii and R. rickettsia. In this work, for the first time, a holistic, consistent and multidimensional observation of a set of closely related bacteria (a family of bacteria) and the  manifestations associated with them was carried out. The basis of  the developed and herein described systematic approach to the  study of bacteria is a new mathematical model — the arrangement of nucleotides in a complete genome and its sensitive  unambiguous numerical characteristics. A new methodological  approach named genomosystematics and based on mathematical  modeling of complete genomes of rickettsiae (bacteria) using FOA.  Classification of rickettsiae and rickettsioses obtained with the help  of this approach corresponds to ecological, epidemiological and  etiological principles. Application of the genomosystematics can  serve the goals and objectives of preventive medicine. The  publication completes a series of scientific works presenting the  methodology of an integrated approach based on the application of  mathematical analysis tools in the study of objects and laws of  natural science disciplines of biological and medical profile.

About the authors

S. N. Shpynov

N.F. Gamaleya National Research Center of Epidemiology and Microbiology

Author for correspondence.
Email: stan63@inbox.ru

PhD, MD (Medicine), Head of Laboratory of Ecology of Rickettsie

123098, Russian Federation, Moscow, Gamaleya str., 18

Phone/fax: +7 (499) 193-61-85 (office)

Russian Federation

N. N. Pozdnichenko

Omsk State Technical University

Email: fake@neicon.ru

Senior Lecturer, Informatics and Computer Engineering Department

Russian Federation

A. S. Gumenyuk

Omsk State Technical University

Email: fake@neicon.ru

PhD (Engineering Sciences), Associate Professor, Informatics and Computer Engineering Department

Russian Federation

A. A. Skiba

Omsk State Technical University

Email: fake@neicon.ru

Software Developer, Informatics and Computer Engineering Department

 

Russian Federation

References

  1. Балашов Ю.С., Дайтер А.Б. Кровососущие членистоногие и риккетсии. Л.: Наука, 1973. 251 с. [Balashov Yu.S., Daiter A.B. Krovososushchie chlenistonogie i rikketsii [Blood- sucking arthropods and rickettsias]. Leningrad: Nauka, 1973. 251 p.]
  2. Громашевский Л.В. Общая эпидемиология. М.: Медицина, 1965. 290 с. [Gromashevskii L.V. Obshchaya epidemiologiya [General epidemiology]. Moscow: Meditsina, 1965. 290 p.]
  3. Гуменюк А.С., Поздниченко Н.Н., Родионов И.Н., Шпынов С.Н. О средствах формального анализа строя нуклеотидных цепей // Математическая биология и биоинформатика. 2013. Т. 8, № 1. С. 373–397. [Gumenyuk A.S., Postnichenko N.N., Rodionov I.N., Shpynov S.N. On the formal analysis of the building of nucleotide chains. Matematicheskaya biologiya i bioinformatika = Mathematical Biology and Bioinformatics, 2013, vol. 8, no. 1, pp. 373–397. doi: 10.17537/2013.8.373 (In Russ.)]
  4. Гуменюк А.С., Поздниченко Н.Н., Скиба А.А., Шпынов С.Н. Программа ЭВМ «Матрица сходства нуклеотидных последовательностей по их компонентам». Свидетельство о Государственной регистрации программы ЭВМ в Реестре программ ЭВМ № 2017616679 от 09.06.2017 г. [Gumenuk A.S., Pozdnichenko N.N., Skiba A.A., Shpynov S.N. Computer Program «Matrix of similarity of nucleotide sequences by their components». Certificate of State Registration of the Computer Program in the Register of Computer Programs № 2017616679, 09.06.2017]
  5. Гуменюк А.С., Поздниченко Н.Н., Скиба А.А., Шпынов С.Н. Программа ЭВМ «Карта генов». Свидетельство о Государственной регистрации программы ЭВМ в Реестре программ ЭВМ № 2017616730 от 13.06.2017 г. [Gumenuk A.S., Pozdnichenko N.N., Skiba A.A., Shpynov S.N. Computer Program «Map of genes». Certificate of State Registration of the Computer Program in the Register of Computer Programs No. 2017616730, 13.06.2017]
  6. Здродовский П.Ф., Голиневич Е.М. Учение о риккетсиях и риккетсиозах. 3-е изд., перераб. и доп. М.: Медицина, 1972. 496 с. [Zdrodovskii P.F., Golinevich E.M. Uchenie o rikketsiyakh i rikketsiozakh. 3-e izd., pererab. i dop. [The doctrine of rickett sias and rickettsiosis. 3rd edition revised and enlarged]. Moscow: Medicina, 1972. 496 p.]
  7. Игнатович В.Ф. Антигенные связи риккетсий Провачека и риккетсий Канада, установленные при изучении сывороток больных болезнью Брилля // Журнал гигиены, эпидемиологии, микробиологии и иммунологии. 1977. T. 21, № 1. C. 48–52. [Ignatovich V.F. Antigenic relations of Rickettsia of Prowazeki and Rickettsia Canada established in the study of sera of patients with Brill’s disease. Zhurnal gigieny, epidemiologii, mikrobiologii i immunologii = Journal of Hygiene, Epidemiology, Microbiology and Immunology, 1977, vol. 21, no. 1, pp. 48–52. (In Russ.)]
  8. Мазур М. Качественная теория информации. М.: Мир, 1974. 240 с. [Mazur M. Kachestvennaya teoriya informatsii. [Qualitative theory of information]. Moscow: Mir, 1974. 240 p.]
  9. Марков А.В., Захаров И.А. Использование количественных мер сходства генных порядков для построения филогенетических реконструкций на примере бактерий рода Rickettsia // Генетика. 2008. Т. 44, № 4. С. 456–466. [Markov A.V., Zakharov I.A. Application of quantitative measures of gene order similarity to phylogenetic reconstructions for bacteria’s of the genus Rickettsia. Genetika = Genetics, 2008, vol. 44, no. 4, pp. 456–466. (In Russ.)]
  10. Павловский Е.Н. Основные положения учения о природной очаговости болезней. Эпидемиология и принципы борьбы с инфекционными болезнями. М.: Медицина, 1965, c. 285–308. [Pavlovskii E.N. Osnovnye polozheniya ucheniya o prirodnoi ochagovosti boleznei. Epidemiologiya i printsipy bor’by s infektsionnymi boleznyami [The main provisions of the doctrine of natural foci of disease. Epidemiology and principles of infectious disease control]. Moscow: Meditsina, 1965, pp. 285–308]
  11. Шпынов С.Н., Гуменюк А.С., Поздниченко Н.Н. Применение числовой характеристики строя нуклеотидов в геномах прокариот для реклассификации внутри рода Rickettsia // Математическая биология и биоинформатика. 2016. Т. 11, № 2. С. 87– 101. [Shpynov S.N., Gumenuk A.S., Pozdnichenko N.N. Application of the numerical characteristic of formal order analysis of the prokaryotic genomes for reclassification within the genus Rickettsia. Matematicheskaya biologiya i bioinformatika = Mathematical Biology and Bioinformatics, 2016, vol. 11, no. 2, pp. 336–350. doi: 10.17537/2016.11.336 (In Russ.)]
  12. Abarca K., Lopez J., Acosta-Jamett G., Martínez-Valdebenito C. Rickettsia felis in Rhipicephalus sanguineus from two distant Chilean cities. Vector Borne Zoonotic Dis., 2013, vol. 13, iss. 8, pp. 607–609. doi: 10.1089/vbz.2012.1201
  13. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol., 1990, vol. 215, no. 3, pp. 403–410. doi: 10.1016/S0022-2836(05)80360-2
  14. Angelakis E., Mediannikov O., Parola P., Raoult D. Rickettsia felis: the complex journey of an emergent human pathogen. Trends Parasitol., 2016, vol. 32, iss. 7, pp. 554–564. doi: 10.1016/j.pt.2016.04.009
  15. Anstead C.A., Chilton N.B. A novel Rickettsia species detected in vole ticks (Ixodes angustus) from Western Canada. Appl. Environ. Microbiol., 2013, vol. 79, no. 24, pp. 7583–7589. doi: 10.1128/AEM.02286-13
  16. Azad A.F. Epidemiology of murine typhus. Ann. Rev. Entomol., 1990, vol. 35, pp. 553–569. doi: 10.1146/annurev.en.35.010190.003005
  17. Azad A.F., Radulovic S., Higgins J.A., Noden B.H., Troyer J.M. Flea-borne rickettsioses: ecologic considerations. Emerg. Infect. Dis., 1997, vol. 3, no. 3, pp. 319–327. doi: 10.3201/eid0303.970308
  18. Bechah Y., Capo C., Mege J.L., Raoult D. Epidemic typhus. Lancet Infect. Dis., 2008, vol. 8, iss. 7, pp. 417–426. doi: 10.1016/S1473-3099(08)70150-6
  19. Bechah Y., Karkouri K.E., Mediannikov O., Leroy Q., Pelletier N., Robert C., Médigue C., Mege J.L., Raoult D. Genomic, proteomic, and transcriptomic analysis of virulent and avirulent Rickettsia prowazekii reveals its adaptive mutation capabilities. Genome Res., 2010, vol. 20, no. 5, pp. 655–663. doi: 10.1101/gr.103564.109
  20. Bishop-Lilly K.A., Ge H., Butani A., Osborne B., Verratti K., Mokashi V., Nagarajan N., Pop M., Read T.D., Richards A.L. Genome sequencing of four strains of Rickettsia prowazekii, the causative agent of epidemic typhus, including one flying squirrel isolate. Genome Announc, 2013, vol. 1, no. 3: e00399-13. doi: 10.1128/genomeA.00399-13
  21. Choi Y.-J., Lee E.-M., Park J.-M., Lee K.-M., Han S.-H., Kim J.-K., Lee S.-H., Song H.-J., Choi M.-S., Kim I.-S., Park K.-H., Jang W.-J. Molecular detection of various Rickettsiae in mites (Acari: Trombiculidae) in southern Jeolla Province, Korea. Microbiol. Immunol., 2007, vol. 51, iss. 3, pp. 307–312. doi: 10.1111/j.1348-0421.2007.tb03912.x
  22. Civen R., Ngo V. Murine typhus: an unrecognized suburban vectorborne disease. Clin. Infect. Dis., 2008, vol. 46, iss. 6, pp. 913–918. doi: 10.1086/527443
  23. Clark T.R., Noriea N.F., Bublitz D.C., Ellison D.W., Martens C., Lutter E.I., Hackstadt T. Comparative genome sequencing of Rickettsia rickettsii strains that differ in virulence. Infect. Immun., 2015, vol. 83, no. 4, pp. 1568–1576. doi: 10.1128/IAI.03140-14
  24. Dieme C., Bechah Y., Socolovschi C., Audoly G., Berenger J.M., Faye O., Raoult D., Parola P. Transmission potential of Rickettsia felis infection by Anopheles gambiae mosquitoes. Proc. Natl. Acad. Sci. USA, 2015, vol. 112, no. 26, pp. 8088–8093. doi: 10.1073/pnas.1413835112
  25. Eisen J.A., Fraser C.M. Phylogenomics: intersection of evolution and genomics. Science, 2003, vol. 300, iss. 5626, pp. 1706–1707. doi: 10.1126/science.1086292
  26. Eremeeva M.E., Dasch G.A., Silverman D.J. Quantitative analyses of variations in the injury of endothelial cells elicited by 11 isolates of Rickettsia rickettsii. Clin. Diagn. Lab. Immunol., 2001, vol. 8, no. 4, pp. 788–796. doi: 10.1128/CDLI.8.4.788-796.2001
  27. Felsheim R.F., Kurtti T.J., Munderloh U.G. Genome sequence of the endosymbiont Rickettsia peacockii and comparison with virulent Rickettsia rickettsii: identification of virulence factors. PLoS One, 2009, vol. 4, iss. 12: e8361. doi: 10.1371/journal.pone.0008361
  28. Fournier P.-E., Dumler J.S., Greub G., Zhang J., Wu Y., Raoult D. Gene sequence-based criteria for identification of new rickett sia isolates and description of Rickettsia heilongjiangensis sp. nov. J. Clin. Microbiol., 2003, vol. 41, no. 12, pp. 5456–5465. doi: 10.1128/JCM.41.12.5456-5465.2003
  29. Fournier P.-E., Raoult D. Current knowledge on phylogeny and taxonomy of Rickettsia spp. Ann. N. Y. Acad. Sci., 2009, vol. 1166, iss. 1, pp. 1–11. doi: 10.1111/j.1749-6632.2009.04528.x
  30. Gillespie J.J., Beier M.S., Rahman M.S., Ammerman N.C., Shallom J.M., Purkayastha A., Sobral B.S., Azad A.F. Plasmids and rickettsial evolution: insight from Rickettsia felis. PLoS One, 2007, iss. 3: e266. doi: 10.1371/journal.pone.0000266
  31. Gillespie J.J., Williams K., Shukla M., Snyder E.E., Nordberg E.K., Ceraul S.M., Dharmanolla C., Rainey D., Soneja J., Shallom J.M., Vishnubhat N.D., Wattam R., Purkayastha A., Czar M., Crasta O., Setubal J.C., Azad A.F., Sobral B.S. Rickettsia phylogenomics: unwinding the intricacies of obligate intracellular life. PLoS One, 2008, vol. 3, iss. 4: e2018. doi: 10.1371/journal.pone.0002018
  32. Ishikura M., Ando S., Shinagawa Y., Matsuura K., Hasegawa S., Nakayama T., Fujita H., Watanabe M. Phylogenetic analysis of spotted fever group rickettsiae based on gltA, 17- kDa, and rOmpA genes amplified by nested PCR from ticks in Japan. Microbiol. Immunol., 2003, vol. 47, no. 11, pp. 823–832. doi: 10.1111/j.1348-0421.2003.tb03448.x
  33. Jado I., Oteo J.A., Aldámiz M., Gil H., Escudero R., Ibarra V., Portu J., Portillo A., Lezaun M.J., García-Amil C., Rodríguez-Moreno I., Anda P. Rickettsia monacensis and human disease, Spain. Emerg. Infect. Dis., 2007, vol. 13, no. 9, pp. 1405–1407. doi: 10.3201/eid1309.060186
  34. Jiang J., Maina A.N., Knobel D.L., Cleaveland S., Laudisoit A., Wamburu K. Molecular detection of Rickettsia felis and Candidatus Rickettsia asemboensis in fleas from human habitats, Asembo, Kenya. Vector Borne Zoonotic Dis., 2013, vol. 13, iss. 8, pp. 550–558. doi: 10.1089/vbz.2012.1123
  35. Koonin E.V., Mushegian A.R., Galperin M.Y., Walker D.R. Comparison of archaeal and bacterial genomes: computer analysis of protein sequences predicts novel functions and suggests a chimeric origin for the archaea. Mol. Microbiol., 1997, vol. 25, iss. 4, pp. 619–637. doi: 10.1046/j.1365-2958.1997.4821861.x
  36. Krantz G.W., Walter D.E. A manual of acarology. 3rd ed. Lubbock: Texas Tech University Press, 2009. 807 p.
  37. Kumar S., Stecher G., Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol., 2016, vol. 33, iss. 7, pp. 1870–1874. doi: 10.1093/molbev/msw054
  38. Linnemann C.C., Petzman C.I., Peterson E.D. Acute febrile cerebrovasculitis. A non-spotted fever group rickettsial disease. Arch. Intern. Med., 1989, vol. 149, no. 7, pp. 1682– 1684. doi: 10.1001/archinte.1989.00390070182031
  39. Mediannikov O., Aubadie-Ladrix M., Raoult D. Candidatus ‘Rickettsia senegalensis’ in cat fleas in Senegal. New Microbes New Infect., 2015, vol. 3, pp. 24–28. doi: 10.1016/j.nmni.2014.10.005
  40. Merhej V., Angelakis E., Socolovschi C., Raoult D. Genotyping, evolution and epidemiological findings of Rickettsia species. Infect. Genet. Evol., 2014, vol. 25, pp. 122– 137. doi: 10.1016/j.meegid.2014.03.014
  41. Merhej V., Raoult D. Rickettsial evolution in the light of comparative genomics. Biol. Rev. Camb. Philos. Soc., 2011, vol. 86, iss. 2, pp. 379–405. doi: 10.1111/j.1469-185X.2010.00151.x
  42. Nichols E., Rindge M.E., Russell G.G. The relationship of the habits of the house mouse and the mouse mite (Allodermanyssus sanguineus) to the spread of rickettsialpox. Ann. Intern. Med., 1953, vol. 39, no. 1, pp. 92–102. doi: 10.7326/0003-4819-39-1-92
  43. Nicholson W.L., Allen K.E., McQuiston J.H., Breitschwerdt E.B., Little S.E. The increasing recognition of rickettsial pathogens in dogs and people. Trends Parasitol., 2010, vol. 26, iss. 4, pp. 205–212. doi: 10.1016/j.pt.2010.01.007
  44. Oliveira K.A., Oliveira L.S., Dias C.C.A., Silva Jr.A., Almeida M.R., Almada G., Bouyer D.H., Galvão M.A.M., Mafra C.L. Molecular identification of Rickettsia felis in ticks and fleas from an endemic area for Brazilian Spotted Fever. Mem. Inst. Oswaldo Cruz, 2008, vol. 103, no. 2, pp. 191–194. doi: 10.1590/S0074-02762008000200011
  45. Parola P., Paddock C.D., Socolovschi C., Labruna M.B., Mediannikov O., Kernif T., Abdad M.Y., Stenos J., Bitam I., Fournier P.-E., Raoult D. Update on tick-borne rickettsioses around the world: a geographic approach. Clin. Microbiol. Rev., 2013, vol. 26, no. 4, pp. 657–702. doi: 10.1128/CMR.00032-13
  46. Prusinski M.A., White J.L., Wong S.J., Conlon M.A., Egan C., Kelly-Cirino C.D., Laniewicz B.R., Backenson P.B., Nicholson W.L., Eremeeva M.E., Karpathy S.E., Dasch G.A., White D.J. Sylvatic typhus associated with flying squirrels (Glaucomys volans) in New York State, United States. Vector Borne Zoonotic Dis., 2014, vol. 14, iss. 4, pp. 240–244. doi: 10.1089/vbz.2013.1392
  47. Raoult D., Roux V. Rickettsioses as paradigms of new or emerging infectious diseases. Clin. Microbiol. Rev., 1997, vol. 10, no. 4, pp. 694–719.
  48. Reif K.E., Macaluso K.R. Ecology of Rickettsia felis: a review. J. Med. Entomol., 2009, vol. 46, no. 4, pp. 723–736.
  49. Shpynov S., Fournier P.-E., Pozdnichenko N., Gumenyuk A., Skiba A. New approaches in the systematics of Rickettsiae. New Microbes New Infect., 2018, vol. 23, pp. 93–102. doi: 10.1016/j.nmni.2018.02.012
  50. Shpynov S., Pozdnichenko N., Gumenuk A. Approach for classification and taxonomy within family Rickettsiaceae based on the Formal Order Analysis. Microbes Infect., 2015, vol. 17, iss. 11–12, pp. 839–844. doi: 10.1016/j.micinf.2015.09.012
  51. Simser J.A., Rahman M.S., Dreher-Lesnick S.M., Azad A.F. A novel and naturally occurring transposon, ISRpe1 in the Rickettsia peacockii genome disrupting the rickA gene involved in actin-based motility. Mol. Microbiol., 2005, vol. 58, iss. 1, pp. 71–79. doi: 10.1111/j.1365-2958.2005.04806.x
  52. Soares H.S., Barbieri A.R.M., Martins T.F., Minervino A.H.H., de Lima J.T.R., Marcili A., Gennari S.M., Labruna M.B. Ticks and rickettsial infection in the wildlife of two regions of the Brazilian Amazon. Exp. Appl. Acarol., 2015, vol. 65, iss. 1, pp. 125–140. doi: 10.1007/s10493-014-9851-6
  53. Socolovschi C., Mediannikov O., Raoult D., Parola P. The relationship between spotted fever group Rickettsiae and ixodid ticks. Vet. Res., 2009, vol. 40, no. 4: 34. doi: 10.1051/vetres/2009017
  54. Socolovschi C., Pages F., Ndiath M.O., Ratmanov P., Raoult D. Rickettsia species in African Anopheles mosquitoes. PLoS One, 2012, vol. 7, iss. 10: e48254. doi: 10.1371/journal.pone.0048254
  55. Stothard D.R., Clark J.B., Fuerst P.A. Ancestral divergence of Rickettsia bellii from the spotted fever and typhus groups of Rickettsia and antiquity of the genus Rickettsia. Int. J. Syst. Bacteriol., 1994, vol. 44, iss. 4, pp. 798–804. doi: 10.1099/00207713-44-4-798
  56. Tamura A., Ohashi N., Urakami H., Miyamura S. Classification of Rickettsia tsutsugamushi in a new genus, Orientia gen. nov., as Orientia tsutsugamushi comb. nov. Int. J. Syst. Bacteriol., 1995, vol. 45, iss. 3, pp. 589–591. doi: 10.1099/00207713-45-3-589
  57. Traub R., Wisseman C.L.Jr. The ecology of chigger-borne rickettsiosis (scrub typhus). J. Med. Entomol., 1974, vol. 11, iss. 3, pp. 237–303. doi: 10.1093/jmedent/11.3.237
  58. Traub R., Wisseman C.L.Jr, Farhang-Azad A. The ecology of murine typhus: a critical review. Trop. Dis. Bull., 1978, vol. 75, no. 4, pp. 237–317.
  59. Weiss E., Moulder J.W. Order I. Rickettsiales, Gieszczkiewicz 1939. Bergey’s manual of systematic bacteriology. Baltimore: Williams and Wilkins, 1984, vol. 1, pp. 687–703.
  60. Wisseman Ch.L.Jr. Observation on global aspects of louse-borne typhus transmission and potential. Proc. Intern. Symp. The control of lice and louse-borne diseases. Washington, 1973, pp. 60–66.
  61. Zemtsova G., Killmaster L.F., Mumcuoglu K.Y., Levin M.L. Co-feeding as a route for transmission of Rickettsia conorii israelensis between Rhipicephalus sanguineus ticks. Exp. Appl. Acarol., 2010, vol. 52, no. 4, pp. 383–392. doi: 10.1007/s10493-010-9375-7

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2018 Shpynov S.N., Pozdnichenko N.N., Gumenyuk A.S., Skiba A.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies