Abstract
Vector-borne microbes are subject to the ecological constraints of two distinct microenvironments: that in the arthropod vector and that in the blood of its vertebrate host. Because the structure of bacterial communities in these two microenvironments may substantially affect the abundance of vector-borne microbes, it is important to understand the relationship between bacterial communities in both microenvironments and the determinants that shape them. We used pyrosequencing analyses to compare the structure of bacterial communities in Synosternus cleopatrae fleas and in the blood of their Gerbillus andersoni hosts. We also monitored the interindividual and seasonal variability in these bacterial communities by sampling the same individual wild rodents during the spring and again during the summer. We show that the bacterial communities in each sample type (blood, female flea or male flea) had a similar phylotype composition among host individuals, but exhibited seasonal variability that was not directly associated with host characteristics. The structure of bacterial communities in male fleas and in the blood of their rodent hosts was remarkably similar and was dominated by flea-borne Bartonella and Mycoplasma phylotypes. A lower abundance of flea-borne bacteria and the presence of Wolbachia phylotypes distinguished bacterial communities in female fleas from those in male fleas and in rodent blood. These results suggest that the overall abundance of a certain vector-borne microbe is more likely to be determined by the abundance of endosymbiotic bacteria in the vector, abundance of other vector-borne microbes co-occurring in the vector and in the host blood and by seasonal changes, than by host characteristics.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
Accession codes
References
Abramsky Z, Brand S, Rosenzweig ML . (1985). Geographical ecology of gerbilline rodents in sand dune habitats of Israel. J Biogeogr 12: 363–372.
Aksoy S . (2000). Tsetse, a haven for microorganisms. Parasitol Today 16: 114–118.
Alexy KJ, Gassett JW, Osborn DA, Miller KV, Russell SM . (2003). Bacterial fauna of the tarsal tufts of white-tailed deer (Odocoileus virginianus). Am Midl Nat 149: 237–240.
Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P . (2006). Seasonality and the dynamics of infectious diseases. Ecol Lett 9: 467–484.
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
Andreotti R, de Leon AAP, Dowd SE, Guerrero FD, Bendele KG, Scoles GA . (2011). Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol 11: 6.
Azad AF, Beard CB . (1998). Rickettsial pathogens and their arthropod vectors. Emerg Infect Dis 4: 179–186.
Bar Y, Abramsky Z, Gutterman Y . (1981). Diet of gerbilline rodents in the Israeli Desert. J Arid Environ 7: 371–376.
Beachey EH . (1980) Bacterial Adherence. Kluwer Academic Publishers: Dordrecht, The Netherlands.
Bottomley PJ, Cheng HH, Strain SR . (1994). Genetic structure and symbiotic characteristics of a Bradyrhizobium population recovered from a pasture soil. Appl Environ Microbiol 60: 1754–1761.
Burnham KP, Anderson DR . (2002) Model Selection and Multimodel Inference. A Practical Information-Theoretic Approach 2 edn. Springer Science and Business Media: New York.
Chomel BB, Boulouis HJ, Breitschwerdt EB, Kasten RW, Vayssier-Taussat M, Birtles RJ et al. (2009). Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Vet Res 40: 29.
Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M et al. (2011). Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332: 855–858.
Clarke KR . (1993). Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117–143.
Clay K, Fuqua C, Lively CM, Wade MJ . (2006). Microbial community ecology of tick-borne human pathogens. In: Collinge SK, Ray C, (eds) Disease Ecology: Community Structure and Pathogen Dynamics. Oxford University Press: Oxford, pp 41–57.
Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R . (2009). Bacterial community variation in human body habitats across space and time. Science 326: 1694–1697.
Coster ME, Stiles J, Krohne SG, Raskin RE . (2008). Results of diagnostic ophthalmic testing in healthy guinea pigs. J Am Vet Med Assoc 232: 1825–1833.
Cox FEG . (2001). Concomitant infections, parasites and immune responses. Parasitology 122: S23–S38.
Cullen CL . (2003). Normal ocular features, conjunctival microflora and intraocular pressure in the Canadian beaver (Castor canadensis). Vet Ophthalmol 6: 279–284.
de la Fuente J, Blouin EF, Kocan KM . (2003). Infection exclusion of the rickettsial pathogen Anaplasma marginale in the tick vector Dermacentor variabilis. Clin Diagn Lab Immunol 10: 182–184.
Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL et al. (2013). The long-term stability of the human gut microbiota. Science 341: 44-+.
Fierer N, Hamady M, Lauber CL, Knight R . (2008). The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105: 17994–17999.
Fisher RA, Cobet AS, Williams CB . (1943). The relation between the number of species and the number of individals in a random sample of an animal population. J Anim Ecol 12: 42–58.
Gavish Y, Kedem H, Messika I, Cohen C, Toh E, Munro D et al. (2014). Association of host and microbial species diversity across spatial scales in desert rodent communities. PLoS One 9: e109677.
Gill JJ, Sabour PM, Gong JH, Yu H, Leslie KE, Griffiths MW . (2006). Characterization of bacterial populations recovered from the teat canals of lactating dairy and beef cattle by 16S rRNA gene sequence analysis. FEMS Microbiol Ecol 56: 471–481.
Godoy-Vitorino F, Goldfarb KC, Brodie EL, Garcia-Amado MA, Michelangeli F, Dominguez-Bello MG . (2010). Developmental microbial ecology of the crop of the folivorous hoatzin. ISME J 4: 611–620.
Gonzalez-Ceron L, Santillan F, Rodriguez MH, Mendez D, Hernandez-Avila JE . (2003). Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J Med Entomol 40: 371–374.
Gorham CH, Fang QQ, Durden LA . (2003). Wolbachia endosymbionts in fleas (Siphonaptera). J Parasitol 89: 283–289.
Grassly NC, Fraser C . (2006). Seasonal infectious disease epidemiology. Proc Biol Sci 273: 2541–2550.
Grice EA, Segre JA . (2011). The skin microbiome. Nat Rev Microbiol 9: 244–253.
Gutiérrez R, Moric D, Cohen C, Hawlena H, Harrus S . (2014). The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas. ISME J 8: 1598–1608.
Gutiérrez R, Morick D, Cohen C, Hawlena H, Harrus S . (2014). The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas. ISME J 8: 1598–1608.
Hawlena H, Abramsky Z, Krasnov BR . (2005). Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146: 200–208.
Hawlena H, Abramsky Z, Krasnov BR . (2006). Ectoparasites and age-dependent survival in a desert rodent. Oecologia 148: 30–39.
Hawlena H, Bashey F, Lively CM . (2012). Bacteriocin-mediated interactions within and between coexisting species. Ecol Evol 2: 2516–2521.
Hawlena H, Rynkiewicz E, Toh E, Alfred A, Durden LA, Hastriter MW et al. (2013). The arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks. ISME J 7: 221–223.
Heise SR, Elshahed MS, Little SE . (2010). Bacterial diversity in Amblyomma americanum (Acari: Ixodidae) with a focus on members of the genus Rickettsia. J Med Entomol 47: 258–268.
Hoffmann AR, Patterson AP, Diesel A, Lawhon SD, Ly HJ, Stephenson CE et al. (2014). The skin microbiome in healthy and allergic dogs. PloS One 9: e83197.
Hornok S, Foldvari G, Elek V, Naranjo V, Farkas R, de la Fuente J . (2008). Molecular identification of Anaplasma marginale and rickettsial endosymbionts in blood-sucking flies (Diptera : Tabanidae, Muscidae) and hard ticks (Acari : Ixodidae). Vet Parasitol 154: 354–359.
Hubbell SP . (2001) The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press: Princeton, NJ.
Hudson PJ, Dobson AP . (1997). Host-parasite processes and demographic consequences. In: Clayton DH, Moore J, (eds) Host-Parasite Evolution. General Principles and Avian Models. Oxford University Press: New York, pp 128–154.
Jaccard P . (1912). The distribution of the flora in the alpine zone. New Phytol 11: 37–50.
Jones RT, Knight R, Martin AP . (2010). Bacterial communities of disease vectors sampled across time, space, and species. ISME J 4: 223–231.
Kedem H, Cohen C, Messika I, Einav M, Pilosof S, Hawlena H . (2014). Multiple effects of host species diversity on co-existing host-specific and host-opportunistic microbes. Ecology 95: 1173–1183.
Kirstein F, Rijpkema S, Molkenboer M, Gray JS . (1997). Local variations in the distribution and prevalence of Borrelia burgdorferi sensu lato genomospecies in Ixodes ricinus ticks. Appl Environ Microbiol 63: 1102–1106.
Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R et al. (2011). Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 108: 4578–4585.
Konig H . (2006). Bacillus species in the intestine of termites and other soil invertebrates. J Appl Microbiol 101: 620–627.
Krasnov BR, Burdelova NV, Shenbrot GI, Khokhlova IS . (2002). Annual cycles of four flea species in the central Negev desert. Med Vet Entomol 16: 266–276.
Krasnov BR, Stanko M, Morand S . (2006). Age-dependent flea (Siphonaptera) parasitism in rodents: a host's life history matters. J Parasitol 92: 242–248.
Krasnov BR . (2008) Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. Cambridge University Press: Cambridge.
Kueneman JG, Parfrey LW, Woodhams DC, Archer HM, Knight R, McKenzie VJ . (2014). The amphibian skin-associated microbiome across species, space and life history stages. Mol Ecol 23: 1238–1250.
Labeda DP, Testa RT, Lechevalier MP, Lechevalier HA . (1984). Saccharothrix: a new genus of the Actinomycetales related to Nocardiopsis. Int J Syst Bacteriol 34: 426–431.
Lalzar I, Harrus S, Mumcuoglu KY, Gottlieb Y . (2012). Composition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial communities. Appl Environ Microbiol 78: 4110–4116.
Leclaire S, Nielsen JF, Drea CM . (2014). Bacterial communities in meerkat anal scent secretions vary with host sex, age, and group membership. Behav Ecol doi:10.1093/beheco/aru109.
Lehmann T . (1989) Population Biology of the Flea Synosternus cleopatra with Emphasis on Host-Parasite Relations (in Hebrew, with English summary). The Hebrew University of Jerusalem: Israel, Jerusalem.
Lemon SM, Sparling PF, Hamburg MA, Relman DA, Choffne ER, Mack A . (2008) Vector-Borne Diseases: Understanding the Environmental, Human Health, and Ecological Connections, Workshop Summary 1st edn vol. 1. National Academies Press: Washington, DC.
Lipsitch M, Siller S, Nowak MA . (1996). The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50: 1729–1741.
Lively CM, Clay K, Wade MJ, Fuqua C . (2005). Competitive co-existence of vertically and horizontally transmitted parasites. Evol Ecol Res 7: 1183–1190.
Macaluso KR, Sonenshine DE, Ceraul SM, Azad AF . (2002). Rickettsial infection in Dermacentor variabilis (Acari : Ixodidae) inhibits transovarial transmission of a second Rickettsia. J Med Entomol 39: 809–813.
Magurran AE . (1988) Ecological Diversity and Its Measurement. Princeton University Press: Princeton, NJ.
Maidak BL, Olsen GJ, Larsen N, Overbeek R, McCaughey MJ, Woese CR . (1996). The Ribosomal Database Project (RDP). Nucleic Acids Res 24: 82–85.
Martin MO, Gilman FR, Weiss SL . (2010). Sex-specific asymmetry within the cloacal microbiota of the striped plateau lizard, Sceloporus virgatus. Symbiosis 51: 97–105.
McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE et al. (2013). Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110: 3229–3236.
Meekins JM, Eshar D, Rankin AJ . (2014). Tear production, intraocular pressure, and conjunctival bacterial flora in a group of captive black-tailed prairie dogs (Cynomys ludovicianus). Vet Ophthalmol doi:10.1111/vop.12226.
Montiani-Ferreira F, Truppel J, Tramontin MH, Vilani RGD, Lange RR . (2008). The capybara eye: clincial tests, anatomic and biometric features. Vet Ophthalmol 11: 386–394.
Mooring MS, Blumstein DT, Stoner CJ . (2004). The evolution of parasite-defence grooming in ungulates. Biol J Linn Soc 81: 17–37.
Moquin SA, Garcia JR, Brantley SL, Takacs-Vesbach CD, Shepherd UL . (2012). Bacterial diversity of bryophyte-dominant biological soil crusts and associated mites. J Arid Environ 87: 110–117.
Moran D, Turner SJ, Clements KD . (2005). Ontogenetic development of the gastrointestinal microbiota in the marine herbivorous fish Kyphosus sydneyanus. Microb Ecol 49: 590–597.
Moreno CX, Moy F, Daniels TJ, Godfrey HP, Cabello FC . (2006). Molecular analysis of microbial communities identified in different developmental stages of Ixodes scapularis ticks from Westchester and Dutchess Counties, New York. Environ Microbiol 8: 761–772.
Morick D, Krasnov BR, Khokhlova IS, Shenbrot GI, Kosoy MY, Harrus S . (2010). Bartonella genotypes in fleas (Insecta: Siphonaptera) collected from rodents in the Negev Desert, Israel. Appl Environ Microbiol 76: 6864–6869.
Morick D, Krasnov BR, Khokhlova IS, Gottlieb Y, Harrus S . (2011). Investigation of Bartonella acquisition and transmission in Xenopsylla ramesis fleas (Siphonaptera: Pulicidae). Mol Ecol 20: 2864–2870.
Morick D, Krasnov BR, Khokhlova IS, Gottlieb Y, Harrus S . (2013). Transmission dynamics of Bartonella sp Strain OE 1-1 in Sundevall's Jirds (Meriones crassus). Appl Environ Microbiol 79: 1258–1264.
Moriyama K, Ando C, Tashiro K, Kuhara S, Okamura S, Nakano S et al. (2008). Polymerase chain reaction detection of bacterial 16S rRNA gene in human blood. Microbiol Immunol 52: 375–382.
Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L et al. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332: 970–974.
Netusil J, Zakovska A, Horvath R, Dendis M, Janouskovcova E . (2005). Presence of Borrelia burgdorferi sensu lato in mites parasitizing small rodents. Vector Borne Zoonotic Dis 5: 227–232.
Noda H, Munderloh UG, Kurtti TJ . (1997). Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl Environ Microbiol 63: 3926–3932.
Oh J, Conlan S, Polley EC, Segre JA, Kong HH . (2012). Shifts in human skin and nares microbiota of healthy children and adults. Genome Med 4: 77.
Olofsson TC, Vasquez A . (2009). Phylogenetic comparison of bacteria isolated from the honey stomachs of honey bees Apis mellifera and bumble bees Bombus spp. J Apic Res 48: 233–237.
Osei-Poku J, Mbogo CM, Palmer WJ, Jiggins FM . (2012). Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol Ecol 21: 5138–5150.
Ostfeld RS . (2009). Climate change and the distribution and intensity of infectious diseases. Ecology 90: 903–905.
Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA et al. (2009). The NIH human microbiome project. Genome Res 19: 2317–2323.
Philip RN, Casper EA, Ormsbee RA, Peacock MG, Burgdorfer W . (1976). Microimmunofluorescence test for serological study of rocky mountain spotted fever and typhus. J Clin Microbiol 3: 51–61.
Pidiyar VJ, Jangid K, Patole MS, Shouche YS . (2004). Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus mosquito midgut based on 16s ribosomal RNA gene analysis. Am J Trop Med Hyg 70: 597–603.
Pumpuni CB, Beier MS, Nataro JP, Guers LD, Davis JR . (1993). Plasmodium falciparum: inhibition of sporogonic development in Anopheles stephensi by gram-negative bacteria. Exp Parasitol 77: 195–199.
Rani A, Sharma A, Rajagopal R, Adak T, Bhatnagar RK . (2009). Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiol 9: 96.
Reed DL, Hafner MS . (2002). Phylogenetic analysis of bacterial communities associated with ectoparasitic chewing lice of pocket gophers: a culture-independent approach. Microb Ecol 44: 78–93.
Reeves WK, Dowling APG, Dasch GA . (2006). Rickettsial agents from parasitic Dermanyssoidea (Acari : Mesostigmata). Exp Appl Acarol 38: 181–188.
Reinhold-Hurek B, Hurek T . (2000). Reassessment of the taxonomic structure of the diazotrophic genus Azoarcus sensu lato and description of three new genera and new species, Azovibrio restrictus gen. nov., sp nov., Azospira oryzae gen. nov., sp nov and Azonexus fungiphilus gen. nov., sp nov. Int J Syst Evol Microbiol 50: 649–659.
Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K et al. (2011). Evidence for a core gut microbiota in the zebrafish. ISME J 5: 1595–1608.
Roper C, Richardson W, Elhassan IM, Giha H, Hviid L, Satti GMH et al. (1998). Seasonal changes in the Plasmodium falciparum population in individuals and their relationship to clinical malaria: a longitudinal study in a Sudanese village. Parasitology 116: 501–510.
Ryan MP, Pembroke JT, Adley CC . (2011). Genotypic and phenotypic diversity of Ralstonia pickettii and Ralstonia insidiosa isolates from clinical and environmental sources including High-purity Water. Diversity in Ralstonia pickettii. BMC Microbiol 11: 194.
Saag P, Tilgar V, Mänd R, Kilgas P, Mägi M . (2011). Plumage bacterial assemblages in a breeding wild passerine: relationships with ecological factors and body condition. Microb Ecol 61: 740–749.
Salminen MK, Rautelin H, Tynkkynen S, Poussa T, Saxelin M, Valtonen V et al. (2004). Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on Probiotic L-Rhamnosus GG. Clin Infect Dis 38: 62–69.
Scarborough CL, Ferrari J, Godfray HCJ . (2005). Aphid protected from pathogen by endosymbiont. Science 310: 1781–1781.
Scharschmidt TC, List K, Grice EA, Szabo R, Program NCS, Renaud G et al. (2009). Matriptase-deficient mice exhibit ichthyotic skin with a selective shift in skin microbiota. J Invest Dermatol 129: 2435–2442.
Schloss PD, Gevers D, Westcott SL . (2011). Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6: e27310.
Sharma P, Sharma S, Maurya RK, De TD, Thomas T, Lata S et al. (2014). Salivary glands harbor more diverse microbial communities than gut in Anopheles culicifacies. Parasit Vectors 7: 235.
Stackebrandt E, Goebel BM . (1994). A place for DNA-DNA reassociation and 16s ribosomal RNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44: 846–849.
Steiner FE, Pinger RR, Vann CN, Abley MJ, Sullivan B, Grindle N et al. (2006). Detection of Anaplasma phagocytophilum and Babesia odocoilei DNA in Ixodes scapularis (Acari: Ixodidae) collected in Indiana. J Med Entomol 43: 437–442.
Steiner FE, Pinger RR, Vann CN, Grindle N, Civitello D, Clay K et al. (2008). Infection and co-infection rates of Anaplasma phagocytophilum variants, Babesia spp., Borrelia burgdorferi, and the rickettsial endosymbiont in Ixodes scapularis (Acari: Ixodidae) from sites in Indiana, Maine, Pennsylvania, and Wisconsin. J Med Entomol 45: 289–297.
Stevens DA, Hamilton JR, Johnson N, Kim KK, Lee JS . (2009). Halomonas, a newly recognized human pathogen causing infections and contamination in a dialysis center three new species. Medicine 88: 244–249.
Sutherst RW . (2004). Global change and human vulnerability to vector-borne diseases. Clin Microbiol Rev 17: 136–173.
Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S et al. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science 330: 243–246.
Tomic-Canic M, Perez-Perez GI, Blumenberg M . (2014). Cutaneous microbiome studies in the times of affordable sequencing. J Dermatol Sci 75: 82–87.
Torsvik V, Goksoyr J, Daae FL . (1990). High diversity in DNA of soil bacteria. Appl Environ Microbiol 56: 782–787.
Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE et al. (2009). A core gut microbiome in obese and lean twins. Nature 457: 480–U487.
Vallet-Gely I, Lemaitre B, Boccard F . (2008). Bacterial strategies to overcome insect defences. Nat Rev Microbiol 6: 302–313.
van Dongen WFD, White J, Brandl HB, Moodley Y, Merkling T, Leclaire S et al. (2013). Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecol 13: 11.
van Overbeek L, Gassner F, van der Plas CL, Kastelein P, Rocha UND, Takken W . (2008). Diversity of Ixodes ricinus tick-associated bacterial communities from different forests. FEMS Microbiol Ecol 66: 72–84.
Voigt CC, Caspers B, Speck S . (2005). Bats, bacteria, and bat smell: Sex-specific diversity of microbes in a sexually selected scent organ. J Mammal 86: 745–749.
Werren JH, Baldo L, Clark ME . (2008). Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741–751.
Wielinga PR, Gaasenbeek C, Fonville M, de Boer A, de Vries A, Dimmers W et al. (2006). Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in the Netherlands. Appl Environ Microbiol 72: 7594–7601.
Willi B, Boretti FS, Cattori V, Tasker S, Meli ML, Reusch C et al. (2005). Identification, molecular characterization, and experimental transmission of a new hemoplasma isolate from a cat with hemolytic anemia in Switzerland. J Clin Microbiol 43: 2581–2585.
Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE et al. (2002). Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP, (eds) The Ecology of Wildlife Disease. Oxford University Press: Oxford, pp 6–44.
Woods JE, Brewer MM, Hawley JR, Wisnewski N, Lappin MR . (2005). Evaluation of experimental transmission of 'Candidatus Mycoplasma haemominutum' and Mycoplasma haemofelis by Ctenocephalides felis to cats. Am J Vet Res 66: 1008–1012.
Woods JE, Wisnewski N, Lappin MR . (2006). Attempted transmission of 'Candidatus Mycoplasma haemominutum' and Mycoplasma haemofelis by feeding cats infected Ctenocephalides felis. Am J Vet Res 67: 494–497.
Worthen PL, Gode CJ, Graf J . (2006). Culture-independent characterization of the digestive-tract microbiota of the medicinal leech reveals a tripartite symbiosis. Appl Environ Microbiol 72: 4775–4781.
Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M et al. (2012). Human gut microbiome viewed across age and geography. Nature 486: 222-+.
Yokota A, Tamura T, Hasegawa T, Huang LH . (1993). Catenuloplanes japonicus gen-nov, sp-nov, nom rev, a new genus of the order Actinomycetales. Int J Syst Bacteriol 43: 805–812.
Yuan DT . (2010). A metagenomic study of the tick midgut. MS thesis, University of Texas: Houston.
Zouache K, Michelland RJ, Failloux AB, Grundmann GL, Mavingui P . (2012). Chikungunya virus impacts the diversity of symbiotic bacteria in mosquito vector. Mol Ecol 21: 2297–2309.
Acknowledgements
We thank M Einav, Z Sigal, E Hyams and A Tsairi for valuable advice during this study. This study was supported by Marie Curie Career Integration Grant Number FP7-293713 and by United States-Israel Binational Science Foundation (Grant Number 2012063). This is publication number 856 of the Mitrani Department of Desert Ecology.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Rights and permissions
About this article
Cite this article
Cohen, C., Toh, E., Munro, D. et al. Similarities and seasonal variations in bacterial communities from the blood of rodents and from their flea vectors. ISME J 9, 1662–1676 (2015). https://doi.org/10.1038/ismej.2014.255
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2014.255
This article is cited by
-
Identification of microbial taxa present in Ctenocephalides felis (cat flea) reveals widespread co-infection and associations with vector phylogeny
Parasites & Vectors (2022)
-
Wolbachia infection dynamics in a natural population of the pear psyllid Cacopsylla pyri (Hemiptera: Psylloidea) across its seasonal generations
Scientific Reports (2022)
-
Ontogeny, species identity, and environment dominate microbiome dynamics in wild populations of kissing bugs (Triatominae)
Microbiome (2020)
-
From endosymbionts to host communities: factors determining the reproductive success of arthropod vectors
Oecologia (2017)
-
Path analyses of cross-sectional and longitudinal data suggest that variability in natural communities of blood-associated parasites is derived from host characteristics and not interspecific interactions
Parasites & Vectors (2015)
