Skip to main content
Erschienen in: EcoHealth 4/2017

01.11.2017 | Original Contribution

Subterranean Mammals: Reservoirs of Infection or Overlooked Sentinels of Anthropogenic Environmental Soiling?

verfasst von: Liezl Retief, Nigel C. Bennett, Jennifer U. M. Jarvis, Armanda D. S. Bastos

Erschienen in: EcoHealth | Ausgabe 4/2017

Einloggen, um Zugang zu erhalten

Abstract

Global reports of emergent pathogens in humans have intensified efforts to identify wildlife reservoirs. Subterranean mammals, such as bathyergid mole rats, are largely overlooked, despite their high-level exposure to soil-dwelling microbes. Initial assessment of bathyergid reservoir potential was determined using a broad-range 16S rRNA PCR approach, which revealed an 83% PCR-positivity for the 234 bathyergid lung samples evaluated. The presence of the Bacillus cereus complex, a ubiquitous bacterial assemblage, containing pathogenic and zoonotic species, was confirmed through nucleotide sequencing, prior to group- and species-specific PCR sequencing. The latter allowed for enhanced placement and prevalence estimations of Bacillus in four bathyergid species sampled across a range of transformed landscapes in the Western Cape Province, South Africa. Two novel Bacillus strains (1 and 2) identified on the basis of the concatenated 16S rRNA-groEL-yeaC data set (2066 nucleotides in length), clustered with B. mycoides (ATCC 6462) and B. weihenstephanensis (WSBC 10204), within a well-supported monophyletic lineage. The levels of co-infection, evaluated with a groEL strain-specific assay, developed specifically for this purpose, were high (71%). The overall Bacillus presence of 17.95% (ranging from 0% for Georychus capensis to 45.35% for Bathyergus suillus) differed significantly between host species (χ2 = 69.643; df = 3; P < 0.05), being significantly higher in bathyergids sampled near an urban informal settlement (χ2 = 70.245; df = 3; P < 0.05). The results highlight the sentinel potential of soil-dwelling mammals for monitoring anthropogenically introduced, opportunistic pathogens and the threats they pose to vulnerable communities, particularly in the developing world.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Ahmod NZ, Gupta RS, Shah HN (2011) Identification of a Bacillus anthracis specific indel in the yeaC gene and development of a rapid pyrosequencing assay for distinguishing B. anthracis from the B. cereus group. Journal of Microbiol Methods 87:278–85; DOI: 10.1016/j.mimet.2011.08.015 [Online September 2, 2011] Ahmod NZ, Gupta RS, Shah HN (2011) Identification of a Bacillus anthracis specific indel in the yeaC gene and development of a rapid pyrosequencing assay for distinguishing B. anthracis from the B. cereus group. Journal of Microbiol Methods 87:278–85; DOI: 10.​1016/​j.​mimet.​2011.​08.​015 [Online September 2, 2011]
Zurück zum Zitat Altman DG, Bland JM (1994) Diagnostic Tests 1: Sensitivity and Specificity. British Medical Journal. 308: 1552–1553. Altman DG, Bland JM (1994) Diagnostic Tests 1: Sensitivity and Specificity. British Medical Journal. 308: 1552–1553.
Zurück zum Zitat Archer, E.K., Bennett, N.C., Ueckermann, E.A., Lutermann, H., 2014. Ectoparasite burdens of the common mole-rat (Cryptomys hottentotus hottentotus) from the Cape Provinces of South Africa. Journal of Parasitology 100, 79–84; DOI:10.1645/13-270.1 Archer, E.K., Bennett, N.C., Ueckermann, E.A., Lutermann, H., 2014. Ectoparasite burdens of the common mole-rat (Cryptomys hottentotus hottentotus) from the Cape Provinces of South Africa. Journal of Parasitology 100, 79–84; DOI:10.​1645/​13-270.​1
Zurück zum Zitat Aujoulat F, Roger F, Bourdier A, Lotthé A, Lamy B, Marchandin H, Jumas-Bilak E (2012) From environment to man: Genome evolution and adaptation of human opportunistic bacterial pathogens. Genes (Basel) 3:191–232; DOI: 10.3390/genes3020191 [Online March 26, 2012] Aujoulat F, Roger F, Bourdier A, Lotthé A, Lamy B, Marchandin H, Jumas-Bilak E (2012) From environment to man: Genome evolution and adaptation of human opportunistic bacterial pathogens. Genes (Basel) 3:191–232; DOI: 10.​3390/​genes3020191 [Online March 26, 2012]
Zurück zum Zitat Bennett NC (2011) Teasing apart socially-induced infertility in non-reproductive female Damaraland mole-rats, Fukomys damarensis (Rodentia: Bathyergidae). Integrative Zoology 6:311–20; DOI: 10.1111/j.1749-4877.2011.00263.x [Online December 20, 2011] Bennett NC (2011) Teasing apart socially-induced infertility in non-reproductive female Damaraland mole-rats, Fukomys damarensis (Rodentia: Bathyergidae). Integrative Zoology 6:311–20; DOI: 10.​1111/​j.​1749-4877.​2011.​00263.​x [Online December 20, 2011]
Zurück zum Zitat Blackburn JK, Van Ert M, Mullins JC, Hadfield TL, Hugh-Jones ME (2014) The necrophagous fly anthrax transmission pathway: empirical and genetic evidence from wildlife epizootics. Vector borne and zoonotic diseases (Larchmont, N.Y.) 14:576–83; DOI: 10.1089/vbz.2013.1538 Blackburn JK, Van Ert M, Mullins JC, Hadfield TL, Hugh-Jones ME (2014) The necrophagous fly anthrax transmission pathway: empirical and genetic evidence from wildlife epizootics. Vector borne and zoonotic diseases (Larchmont, N.Y.) 14:576–83; DOI: 10.​1089/​vbz.​2013.​1538
Zurück zum Zitat Brillard J, Dupont CMS, Berge O, Dargaignaratz C, Oriol-Gagnier S, Doussan C, Broussolle V, Gillon M, Clavel T, Bérard A (2015) The water cycle, a potential source of the bacterial pathogen Bacillus cereus. BioMed Research International 2015:356928; DOI: 10.1155/2015/356928 [Online March 30, 2015] Brillard J, Dupont CMS, Berge O, Dargaignaratz C, Oriol-Gagnier S, Doussan C, Broussolle V, Gillon M, Clavel T, Bérard A (2015) The water cycle, a potential source of the bacterial pathogen Bacillus cereus. BioMed Research International 2015:356928; DOI: 10.​1155/​2015/​356928 [Online March 30, 2015]
Zurück zum Zitat Carlin F, Brillard J, Broussolle V, Clavel T, Duport C, Jobin M, Guinebretière MH, Auger S, Sorokine A, Nguyen-Thé C (2010) Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a changing environment. Food Research International 43: 1885–1894; DOI: 10.1016/j.foodres.2009.10.024 Carlin F, Brillard J, Broussolle V, Clavel T, Duport C, Jobin M, Guinebretière MH, Auger S, Sorokine A, Nguyen-Thé C (2010) Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a changing environment. Food Research International 43: 1885–1894; DOI: 10.​1016/​j.​foodres.​2009.​10.​024
Zurück zum Zitat Cheng T, Lin P, Jin S, Wu Y, Fu B, Long R, Liu D, Guo Y, Peng L, Xia Q (2014) Complete genome sequence of Bacillus bombysepticus, a pathogen leading to Bombyx mori black chest septicemia. Genome Announcements 2(3): e00312–14; DOI: 10.1128/genomeA.00312-14 [Online May 15, 2014] Cheng T, Lin P, Jin S, Wu Y, Fu B, Long R, Liu D, Guo Y, Peng L, Xia Q (2014) Complete genome sequence of Bacillus bombysepticus, a pathogen leading to Bombyx mori black chest septicemia. Genome Announcements 2(3): e00312–14; DOI: 10.​1128/​genomeA.​00312-14 [Online May 15, 2014]
Zurück zum Zitat Cronjé N, Swartz I, Retief L, Bastos ADS, Matthee S, Preiser W, Bennett NC, Maphanga T, Govender TM, Colebunders R, Kenyon C (2017) Attempted molecular detection of the human dimorphic fungal pathogen Emergomyces africanus in rodents and insectivores in South Africa. Medical Mycology; DOI:10.1093/mmy/myx065 Cronjé N, Swartz I, Retief L, Bastos ADS, Matthee S, Preiser W, Bennett NC, Maphanga T, Govender TM, Colebunders R, Kenyon C (2017) Attempted molecular detection of the human dimorphic fungal pathogen Emergomyces africanus in rodents and insectivores in South Africa. Medical Mycology; DOI:10.​1093/​mmy/​myx065
Zurück zum Zitat Davies KC, Jarvis JUM (1986) The burrow systems and burrowing dynamics of the mole-rats Bathyergus suillus and Cryptomys hottentotus in the fynbos of the south-western Cape, South Africa. Journal of Zoology 209:125–147; DOI: 10.1111/j.1469-7998.1986.tb03570.x [Online March 17, 2011] Davies KC, Jarvis JUM (1986) The burrow systems and burrowing dynamics of the mole-rats Bathyergus suillus and Cryptomys hottentotus in the fynbos of the south-western Cape, South Africa. Journal of Zoology 209:125–147; DOI: 10.​1111/​j.​1469-7998.​1986.​tb03570.​x [Online March 17, 2011]
Zurück zum Zitat De Graaff, G (1981) The rodents of southern Africa. Pretoria: Sigma Press (Pty) Ltd. De Graaff, G (1981) The rodents of southern Africa. Pretoria: Sigma Press (Pty) Ltd.
Zurück zum Zitat Didelot X, Barker M, Falush D, Priest FG (2009) Evolution of pathogenicity in the Bacillus cereus group. Systematic and Applied Microbiology 32:81–90; DOI: 10.1016/j.syapm.2009.01.001 [Online February 5, 2009] Didelot X, Barker M, Falush D, Priest FG (2009) Evolution of pathogenicity in the Bacillus cereus group. Systematic and Applied Microbiology 32:81–90; DOI: 10.​1016/​j.​syapm.​2009.​01.​001 [Online February 5, 2009]
Zurück zum Zitat Dragon DC, Rennie RP (1995) The ecology of anthrax spores: tough but not invincible. Canadian Veterinary Journal 36:295–301. Dragon DC, Rennie RP (1995) The ecology of anthrax spores: tough but not invincible. Canadian Veterinary Journal 36:295–301.
Zurück zum Zitat Duran Alvarez JC, Jimenez Cisneros B (2014) Beneficial and negative impacts on soil by the reuse of treated / untreated municipal wastewater for agricultural irrigation – a review of the current knowledge and future perspectives. Environmental risk assessment of soil contamination 137–197; DOI: 10.5772/57086 [Online March 26, 2014] Duran Alvarez JC, Jimenez Cisneros B (2014) Beneficial and negative impacts on soil by the reuse of treated / untreated municipal wastewater for agricultural irrigation – a review of the current knowledge and future perspectives. Environmental risk assessment of soil contamination 137–197; DOI: 10.​5772/​57086 [Online March 26, 2014]
Zurück zum Zitat Edwards U, Rogall T, Blöcker H, Emde M, Böttger, EC (1989) Isolation and direct nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Research 17: 7843–7853; DOI: 10.1093/nar/17.19.7843 Edwards U, Rogall T, Blöcker H, Emde M, Böttger, EC (1989) Isolation and direct nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Research 17: 7843–7853; DOI: 10.​1093/​nar/​17.​19.​7843
Zurück zum Zitat Gale P, Drew T, Phipps LP, David G, Wooldridge M (2009) The effect of climate change on the occurrence and prevalence of livestock diseases in Great Britain. Journal of Applied Microbiology 106:1409–1423; DOI: 10.1111/j.1365-2672.2008.04036.x [Online January 16, 2009] Gale P, Drew T, Phipps LP, David G, Wooldridge M (2009) The effect of climate change on the occurrence and prevalence of livestock diseases in Great Britain. Journal of Applied Microbiology 106:1409–1423; DOI: 10.​1111/​j.​1365-2672.​2008.​04036.​x [Online January 16, 2009]
Zurück zum Zitat Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59: 307–321; DOI:10.1093/sysbio/syq010 [Online March 29, 2010] Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59: 307–321; DOI:10.​1093/​sysbio/​syq010 [Online March 29, 2010]
Zurück zum Zitat Guinebretière MH, Thompson FL, Sorokin A, Normand P, Dawyndt P, Ehling-Schulz M, Svensson B, Sanchis V, Nguyen-The C, Heyndrickx M, De Vos P (2008) Ecological diversification in the Bacillus cereus group. Environmental Microbiology 10:851–865; DOI: 10.1111/j.1462-2920.2007.01495.x [Online November 25, 2007] Guinebretière MH, Thompson FL, Sorokin A, Normand P, Dawyndt P, Ehling-Schulz M, Svensson B, Sanchis V, Nguyen-The C, Heyndrickx M, De Vos P (2008) Ecological diversification in the Bacillus cereus group. Environmental Microbiology 10:851–865; DOI: 10.​1111/​j.​1462-2920.​2007.​01495.​x [Online November 25, 2007]
Zurück zum Zitat Guinebretière MH, Velge P, Couvert O, Carlin F, Debuyser ML, Nguyen-The C (2010) Ability of Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (groups I to VII) rather than species affiliation. Journal of Clinical Microbiology 48:3388–3391; DOI: 10.1128/JCM.00921-10 [Online July 21, 2010] Guinebretière MH, Velge P, Couvert O, Carlin F, Debuyser ML, Nguyen-The C (2010) Ability of Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (groups I to VII) rather than species affiliation. Journal of Clinical Microbiology 48:3388–3391; DOI: 10.​1128/​JCM.​00921-10 [Online July 21, 2010]
Zurück zum Zitat Guinebretière, MH, Auger S, Galleron N, Contzen M, De Sarrau B, De Buyser ML, Lamberet G, Fagerlund A, Granum PE, Lereclus D, De Vos P, Nguyen-The C, Sorokin A (2013) Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus group occasionally associated with food poisoning. International Journal of Systematic and Evolutionary Microbiology 63: 31–40; DOI:10.1099/ijs.0.030627-0 [Online February 10, 2012] Guinebretière, MH, Auger S, Galleron N, Contzen M, De Sarrau B, De Buyser ML, Lamberet G, Fagerlund A, Granum PE, Lereclus D, De Vos P, Nguyen-The C, Sorokin A (2013) Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus group occasionally associated with food poisoning. International Journal of Systematic and Evolutionary Microbiology 63: 31–40; DOI:10.​1099/​ijs.​0.​030627-0 [Online February 10, 2012]
Zurück zum Zitat Halliday JE, Meredith AL, Knobel DL, Shaw DJ, Bronsvoort BM, Cleaveland S (2007) A framework for evaluating animals as sentinels for infectious disease surveillance. Journal of the Royal Society Interface 4:973–984; DOI: 10.1098/rsif.2007.0237. Halliday JE, Meredith AL, Knobel DL, Shaw DJ, Bronsvoort BM, Cleaveland S (2007) A framework for evaluating animals as sentinels for infectious disease surveillance. Journal of the Royal Society Interface 4:973–984; DOI: 10.​1098/​rsif.​2007.​0237.
Zurück zum Zitat Haydon DT, Cleaveland S, Taylor LH, Laurenson MK (2002) Identifying reservoirs of infection a conceptual and practical challenge. Emerging Infectious Diseases 8: 1468–1473; DOI: 10.3201/eid0812.010317. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK (2002) Identifying reservoirs of infection a conceptual and practical challenge. Emerging Infectious Diseases 8: 1468–1473; DOI: 10.​3201/​eid0812.​010317.
Zurück zum Zitat Helgason E, Økstad OA, Dominique A, Johansen H a, Fouet A, Hegna I, Kolstø A, Økstad OLEA, Caugant D a, Mock LE, Hegna IDA (2000) Bacillus anthracis, Bacillus cereus and Bacillus thuringiensis - one species on the basis of genetic evidence. Applied and Environmental Microbiology 66:2627 –2630; DOI: 10.1128/AEM.66.6.2627-2630.2000. Helgason E, Økstad OA, Dominique A, Johansen H a, Fouet A, Hegna I, Kolstø A, Økstad OLEA, Caugant D a, Mock LE, Hegna IDA (2000) Bacillus anthracis, Bacillus cereus and Bacillus thuringiensis - one species on the basis of genetic evidence. Applied and Environmental Microbiology 66:2627 –2630; DOI: 10.​1128/​AEM.​66.​6.​2627-2630.​2000.
Zurück zum Zitat Hubálek Z, Burda H, Scharff A, Heth G, Nevo E, Šumbera R, Pesko J, Zima J (2005) Emmonsiosis of subterranean rodents (Bathyergidae, Spalacidae) in Africa and Israel. Journal of Medical Mycology 43: 691–697; DOI: 10.1080/13693780500179553 Hubálek Z, Burda H, Scharff A, Heth G, Nevo E, Šumbera R, Pesko J, Zima J (2005) Emmonsiosis of subterranean rodents (Bathyergidae, Spalacidae) in Africa and Israel. Journal of Medical Mycology 43: 691–697; DOI: 10.​1080/​1369378050017955​3
Zurück zum Zitat Huelsenbeck JP, Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17:754–755 Huelsenbeck JP, Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17:754–755
Zurück zum Zitat Jackson VA, Paulse AN, Bester AA, Neethling JH, Khan S, Khan W (2009) Bioremediation of metal contamination in the Plankenburg River, Western Cape, South Africa. International Biodeterioration & Biodegradation 63:559–568; DOI: 10.1016/j.ibiod.2009.03.007 Jackson VA, Paulse AN, Bester AA, Neethling JH, Khan S, Khan W (2009) Bioremediation of metal contamination in the Plankenburg River, Western Cape, South Africa. International Biodeterioration & Biodegradation 63:559–568; DOI: 10.​1016/​j.​ibiod.​2009.​03.​007
Zurück zum Zitat Jarvis J, Bennett N (1993) Eusociality has evolved independently in two genera of bathyergid mole-rats—but occurs in no other subterranean mammal. Behavioral Ecology and Sociobiology 33:253–260; DOI: 10.1007/BF02027122 Jarvis J, Bennett N (1993) Eusociality has evolved independently in two genera of bathyergid mole-rats—but occurs in no other subterranean mammal. Behavioral Ecology and Sociobiology 33:253–260; DOI: 10.​1007/​BF02027122
Zurück zum Zitat Jarvis JUM, Bennett NC, Spinks AC (1998) Food availability and foraging by wild colonies of Damaraland mole-rats (Cryptomys damarensis): implications for sociality. Oecologia 113: 290–298. Jarvis JUM, Bennett NC, Spinks AC (1998) Food availability and foraging by wild colonies of Damaraland mole-rats (Cryptomys damarensis): implications for sociality. Oecologia 113: 290–298.
Zurück zum Zitat Jiménez G, Urdiain M, Cifuentes A, López-López A, Blanch AR, Tamames J, Kämpfer P, Kolstø A-B, Ramón D, Martínez JF, Codoñer FM, Rosselló-Móra R (2013) Description of Bacillus toyonensis sp. nov., a novel species of the Bacillus cereus group, and pairwise genome comparisons of the species of the group by means of ANI calculations. Systematic and Applied Microbiology 36:383–391; DOI: 10.1016/j.syapm.2013.04.008 [Online June 19, 2013] Jiménez G, Urdiain M, Cifuentes A, López-López A, Blanch AR, Tamames J, Kämpfer P, Kolstø A-B, Ramón D, Martínez JF, Codoñer FM, Rosselló-Móra R (2013) Description of Bacillus toyonensis sp. nov., a novel species of the Bacillus cereus group, and pairwise genome comparisons of the species of the group by means of ANI calculations. Systematic and Applied Microbiology 36:383–391; DOI: 10.​1016/​j.​syapm.​2013.​04.​008 [Online June 19, 2013]
Zurück zum Zitat Kenyon C, Bonorchis K, Corcoran C, Path FC, Meintjes G, Locketz M, Lehloenya R, Derm FC, Vismer HF, Naicker P, Prozesky H, Van Wyk M, Bamford C, Du Plooy M, Imrie G, Dlamini S, Borman AM, Colebunders R, Yansouni CP, Mendelson M, Govender NP (2013) A dimorphic fungus causing disseminated infection in South Africa. The New England Journal of Medicine 369: 1416–1424; DOI: 10.1056/NEJMoa1215460 [Online October 10, 2013] Kenyon C, Bonorchis K, Corcoran C, Path FC, Meintjes G, Locketz M, Lehloenya R, Derm FC, Vismer HF, Naicker P, Prozesky H, Van Wyk M, Bamford C, Du Plooy M, Imrie G, Dlamini S, Borman AM, Colebunders R, Yansouni CP, Mendelson M, Govender NP (2013) A dimorphic fungus causing disseminated infection in South Africa. The New England Journal of Medicine 369: 1416–1424; DOI: 10.​1056/​NEJMoa1215460 [Online October 10, 2013]
Zurück zum Zitat Lövy M, Šklíba J, Burda H, Chitaukali WN, Šumbera R (2012) Ecological characteristics in habitats of two African mole-rat species with different social systems in an area of sympatry: implications for the mole-rat social evolution. Journal of Zoology 286: 145–153; DOI:10.1111/j.1469-7998.2011.00860.x [Online January 25, 2012] Lövy M, Šklíba J, Burda H, Chitaukali WN, Šumbera R (2012) Ecological characteristics in habitats of two African mole-rat species with different social systems in an area of sympatry: implications for the mole-rat social evolution. Journal of Zoology 286: 145–153; DOI:10.​1111/​j.​1469-7998.​2011.​00860.​x [Online January 25, 2012]
Zurück zum Zitat Nei M, Kumar S (2000) Molecular Evolution and Phylogenetics. Oxford University Press, New York. Nei M, Kumar S (2000) Molecular Evolution and Phylogenetics. Oxford University Press, New York.
Zurück zum Zitat Park S, Kim H, Kim J, Kim T, Kim H (2007) Simultaneous detection and identification of using multiplex PCR group bacteria. Journal of Microbiology and Biotechnology 17: 1177–1182. Park S, Kim H, Kim J, Kim T, Kim H (2007) Simultaneous detection and identification of using multiplex PCR group bacteria. Journal of Microbiology and Biotechnology 17: 1177–1182.
Zurück zum Zitat Paulse AN, Jackson VA, Khan S, Khan W (2012) Isolation and identification of bacterial pollutants from the Berg and Plankenburg Rivers in the Western Cape, South Africa. Water SA 38:819–824; DOI: 10.4314/wsa.v38i5.23 [Online October 5, 2012] Paulse AN, Jackson VA, Khan S, Khan W (2012) Isolation and identification of bacterial pollutants from the Berg and Plankenburg Rivers in the Western Cape, South Africa. Water SA 38:819–824; DOI: 10.​4314/​wsa.​v38i5.​23 [Online October 5, 2012]
Zurück zum Zitat Reysenbach AL, Giver LJ, Wickham GS, Pace NR (1992) Differential amplification of rRNA genes by polymerase chain reaction. Applied and Environmental Microbiology 58: 3417–3418 Reysenbach AL, Giver LJ, Wickham GS, Pace NR (1992) Differential amplification of rRNA genes by polymerase chain reaction. Applied and Environmental Microbiology 58: 3417–3418
Zurück zum Zitat Robb GN, Woodborne S, Bennett, NC (2012) Subterranean sympatry: An investigation into diet using stable isotope analysis. Plos One, 7: 1–10; DOI:10.1371/journal.pone.0048572 [Online November 5, 2012] Robb GN, Woodborne S, Bennett, NC (2012) Subterranean sympatry: An investigation into diet using stable isotope analysis. Plos One, 7: 1–10; DOI:10.​1371/​journal.​pone.​0048572 [Online November 5, 2012]
Zurück zum Zitat Roper TJ, Bennett NC, Conradt L, Molteno AJ (2001) Environmental conditions in burrows of two species of African mole-rat, Georhychus capensis and Cryptomys damarensis. Journal of Zoology 254:101–107; DOI: 10.1017/S0952836901000590 [Online February 28, 2006] Roper TJ, Bennett NC, Conradt L, Molteno AJ (2001) Environmental conditions in burrows of two species of African mole-rat, Georhychus capensis and Cryptomys damarensis. Journal of Zoology 254:101–107; DOI: 10.​1017/​S095283690100059​0 [Online February 28, 2006]
Zurück zum Zitat Saitou, N. & Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–25. Saitou, N. & Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–25.
Zurück zum Zitat Shabbir MZ, Jamil T, Ali AA, Ahmad A, Naeem M, Chaudhary MH, Bilal M, Ali MA, Muhammad K, Yaqub T, Bano A, Mirza AI, Shabbir MAB, Mcvey WR, Patel K, Francesconi S, Jayarao BM, Rabbani M (2015) Prevalence and distribution of soil-borne zoonotic pathogens in Lahore district of Pakistan. Frontiers in Microbiology 6: 1–9; DOI: 10.3389/fmicb.2015.00917 [Online September 10, 2015] Shabbir MZ, Jamil T, Ali AA, Ahmad A, Naeem M, Chaudhary MH, Bilal M, Ali MA, Muhammad K, Yaqub T, Bano A, Mirza AI, Shabbir MAB, Mcvey WR, Patel K, Francesconi S, Jayarao BM, Rabbani M (2015) Prevalence and distribution of soil-borne zoonotic pathogens in Lahore district of Pakistan. Frontiers in Microbiology 6: 1–9; DOI: 10.​3389/​fmicb.​2015.​00917 [Online September 10, 2015]
Zurück zum Zitat Skinner JD, Smithers RHN (1990) The mammals of the Southern African subregion. 2nd edition. Pretoria: University of Pretoria. Skinner JD, Smithers RHN (1990) The mammals of the Southern African subregion. 2nd edition. Pretoria: University of Pretoria.
Zurück zum Zitat Smith KL, De Vos V, Bryden HB, Hugh-Janes ME, Klevytska A, Price LB, Keim P, Scholl DT (1999) Meso-scale ecology of anthrax in Southern Africa: A pilot study of diversity and clustering. Journal of Applied Microbiology 87:204–207; DOI: 10.1046/j.1365-2672.1999.00871.x [Online December 25, 2001] Smith KL, De Vos V, Bryden HB, Hugh-Janes ME, Klevytska A, Price LB, Keim P, Scholl DT (1999) Meso-scale ecology of anthrax in Southern Africa: A pilot study of diversity and clustering. Journal of Applied Microbiology 87:204–207; DOI: 10.​1046/​j.​1365-2672.​1999.​00871.​x [Online December 25, 2001]
Zurück zum Zitat Sparks RE (1995) Need for ecosystem management of large rivers and their floodplains. Bioscience 45:168–182; doi: 10.2307/1312556 Sparks RE (1995) Need for ecosystem management of large rivers and their floodplains. Bioscience 45:168–182; doi: 10.​2307/​1312556
Zurück zum Zitat Streicher, S., Boyles, J.G., Oosthuizen, M.K., Bennett, N.C., 2011. Body temperature patterns and rhythmicity in free-ranging subterranean Damaraland mole-rats, Fukomys damarensis. PLoS One 6, e26346; DOI:10.1371/journal.pone.0026346 Streicher, S., Boyles, J.G., Oosthuizen, M.K., Bennett, N.C., 2011. Body temperature patterns and rhythmicity in free-ranging subterranean Damaraland mole-rats, Fukomys damarensis. PLoS One 6, e26346; DOI:10.​1371/​journal.​pone.​0026346
Zurück zum Zitat Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729; DOI:10.1093/molbev/ mst197 [Online October 16] Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729; DOI:10.​1093/​molbev/ mst197 [Online October 16]
Zurück zum Zitat Thomas HG, Bateman PW, Le Comber SC, Bennett NC, Elwood RW, Scantlebury M (2009) Burrow architecture and digging activity in the Cape dune mole rat. Journal of Zoology 279:277–284; DOI: 10.1111/j.1469-7998.2009.00616.x [Online October 27, 2009] Thomas HG, Bateman PW, Le Comber SC, Bennett NC, Elwood RW, Scantlebury M (2009) Burrow architecture and digging activity in the Cape dune mole rat. Journal of Zoology 279:277–284; DOI: 10.​1111/​j.​1469-7998.​2009.​00616.​x [Online October 27, 2009]
Zurück zum Zitat Thorsen L, Hansen BM, Nielsen KF, Hendriksen NB, Phipps RK, Budde BB (2006) Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Applied and Environmental Microbiology 72:5118–5121; DOI: 10.1128/AEM.00170-06 Thorsen L, Hansen BM, Nielsen KF, Hendriksen NB, Phipps RK, Budde BB (2006) Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Applied and Environmental Microbiology 72:5118–5121; DOI: 10.​1128/​AEM.​00170-06
Zurück zum Zitat Tourasse NJ, Helgason E, Økstad O a., Hegna IK, Kolstø a. B (2006) The Bacillus cereus group: Novel aspects of population structure and genome dynamics. Journal of Applied Microbiology 101:579–593; DOI: 10.1111/j.1365-2672.2006.03087.x [Online July 31, 2006] Tourasse NJ, Helgason E, Økstad O a., Hegna IK, Kolstø a. B (2006) The Bacillus cereus group: Novel aspects of population structure and genome dynamics. Journal of Applied Microbiology 101:579–593; DOI: 10.​1111/​j.​1365-2672.​2006.​03087.​x [Online July 31, 2006]
Zurück zum Zitat Tourasse NJ, Helgason E, Klevan A, Sylvestre P, Moya M, Haustant M, Økstad OA, Fouet A, Mock M, Kolstø AB (2011) Extended and global phylogenetic view of the Bacillus cereus group population by combination of MLST, AFLP, and MLEE genotyping data. Food Microbiology 28:236–244; DOI: 10.1016/j.fm.2010.06.014 [Online July 17, 2010] Tourasse NJ, Helgason E, Klevan A, Sylvestre P, Moya M, Haustant M, Økstad OA, Fouet A, Mock M, Kolstø AB (2011) Extended and global phylogenetic view of the Bacillus cereus group population by combination of MLST, AFLP, and MLEE genotyping data. Food Microbiology 28:236–244; DOI: 10.​1016/​j.​fm.​2010.​06.​014 [Online July 17, 2010]
Zurück zum Zitat Vilain S, Luo Y, Hildreth MB, Brözel VS (2006) Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Applied and Environmental Microbiology 72:4970–4977; DOI: 10.1128/AEM.03076-05 Vilain S, Luo Y, Hildreth MB, Brözel VS (2006) Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Applied and Environmental Microbiology 72:4970–4977; DOI: 10.​1128/​AEM.​03076-05
Zurück zum Zitat Von Stetten F, Mayr R, Scherer S (1999) Climatic influence on mesophilic Bacillus cereus and psychrotolerant Bacillus weihenstephanensis populations in tropical, temperate and alpine soil. Environmental Microbiology 1:503–515; DOI: 10.1046/j.1462-2920 1999.t01-1-00070.x [Online October 13, 2013] Von Stetten F, Mayr R, Scherer S (1999) Climatic influence on mesophilic Bacillus cereus and psychrotolerant Bacillus weihenstephanensis populations in tropical, temperate and alpine soil. Environmental Microbiology 1:503–515; DOI: 10.​1046/​j.​1462-2920 1999.t01-1-00070.x [Online October 13, 2013]
Zurück zum Zitat Zwick ME, Joseph SJ, Didelot X, Chen PE, Bishop-Lilly KA, Stewart AC, Willner K, Nolan N, Lentz S, Thomason MK, Sozhamannan S, Mateczun AJ, Du L, Read TD (2012) Genomic characterization of the Bacillus cereus sensu lato species: Backdrop to the evolution of Bacillus anthracis. Genome Research 22:1512–1524; DOI: 10.1101/gr.134437.111 [Online May 29, 2012] Zwick ME, Joseph SJ, Didelot X, Chen PE, Bishop-Lilly KA, Stewart AC, Willner K, Nolan N, Lentz S, Thomason MK, Sozhamannan S, Mateczun AJ, Du L, Read TD (2012) Genomic characterization of the Bacillus cereus sensu lato species: Backdrop to the evolution of Bacillus anthracis. Genome Research 22:1512–1524; DOI: 10.​1101/​gr.​134437.​111 [Online May 29, 2012]
Metadaten
Titel
Subterranean Mammals: Reservoirs of Infection or Overlooked Sentinels of Anthropogenic Environmental Soiling?
verfasst von
Liezl Retief
Nigel C. Bennett
Jennifer U. M. Jarvis
Armanda D. S. Bastos
Publikationsdatum
01.11.2017
Verlag
Springer US
Erschienen in
EcoHealth / Ausgabe 4/2017
Print ISSN: 1612-9202
Elektronische ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-017-1281-6

Weitere Artikel der Ausgabe 4/2017

EcoHealth 4/2017 Zur Ausgabe