Sodalis glossinidius presence in wild tsetse is only associated with presence of trypanosomes in complex interactions with other tsetse-specific factors

doi:10.1186/s12866-018-1285-6

. 2018 Nov 23;18(Suppl 1):163.

doi: 10.1186/s12866-018-1285-6.

Sodalis glossinidius presence in wild tsetse is only associated with presence of trypanosomes in complex interactions with other tsetse-specific factors

Manun Channumsin^{1

2}, Marc Ciosi^{3

4}, Dan Masiga⁵, C Michael R Turner⁶, Barbara K Mable⁷

Affiliations

¹ Institute of Biodiversity, Animal Health and Comparative Medicine (BAHCM), Graham Kerr Building, University of Glasgow, University Place, Glasgow, G12 8QQ, UK. manun_wo@rmutto.ac.th.
² Faculty of Veterinary Medicine, Rajamangala University of Technology Tawan-Ok, Chonburi, 20110, Thailand. manun_wo@rmutto.ac.th.
³ Institute of Biodiversity, Animal Health and Comparative Medicine (BAHCM), Graham Kerr Building, University of Glasgow, University Place, Glasgow, G12 8QQ, UK. marc.ciosi@glasgow.ac.uk.
⁴ International Centre of Insect Physiology and Ecology (ICIPE), P.O. Box 30772, Nairobi, 00100, Kenya. marc.ciosi@glasgow.ac.uk.
⁵ International Centre of Insect Physiology and Ecology (ICIPE), P.O. Box 30772, Nairobi, 00100, Kenya.
⁶ Institute of Infection, Immunity and Inflammation, Sir Graeme Davis Building, University of Glasgow, University Place, Glasgow, G12 0PT, UK.
⁷ Institute of Biodiversity, Animal Health and Comparative Medicine (BAHCM), Graham Kerr Building, University of Glasgow, University Place, Glasgow, G12 8QQ, UK.

PMID: 30470184
PMCID: PMC6251152
DOI: 10.1186/s12866-018-1285-6

Sodalis glossinidius presence in wild tsetse is only associated with presence of trypanosomes in complex interactions with other tsetse-specific factors

Manun Channumsin et al. BMC Microbiol. 2018.

. 2018 Nov 23;18(Suppl 1):163.

doi: 10.1186/s12866-018-1285-6.

Authors

Manun Channumsin^{1

2}, Marc Ciosi^{3

4}, Dan Masiga⁵, C Michael R Turner⁶, Barbara K Mable⁷

Affiliations

¹ Institute of Biodiversity, Animal Health and Comparative Medicine (BAHCM), Graham Kerr Building, University of Glasgow, University Place, Glasgow, G12 8QQ, UK. manun_wo@rmutto.ac.th.
² Faculty of Veterinary Medicine, Rajamangala University of Technology Tawan-Ok, Chonburi, 20110, Thailand. manun_wo@rmutto.ac.th.
³ Institute of Biodiversity, Animal Health and Comparative Medicine (BAHCM), Graham Kerr Building, University of Glasgow, University Place, Glasgow, G12 8QQ, UK. marc.ciosi@glasgow.ac.uk.
⁴ International Centre of Insect Physiology and Ecology (ICIPE), P.O. Box 30772, Nairobi, 00100, Kenya. marc.ciosi@glasgow.ac.uk.
⁵ International Centre of Insect Physiology and Ecology (ICIPE), P.O. Box 30772, Nairobi, 00100, Kenya.
⁶ Institute of Infection, Immunity and Inflammation, Sir Graeme Davis Building, University of Glasgow, University Place, Glasgow, G12 0PT, UK.
⁷ Institute of Biodiversity, Animal Health and Comparative Medicine (BAHCM), Graham Kerr Building, University of Glasgow, University Place, Glasgow, G12 8QQ, UK.

PMID: 30470184
PMCID: PMC6251152
DOI: 10.1186/s12866-018-1285-6

Abstract

Background: Susceptibility of tsetse flies (Glossina spp.) to trypanosomes of both humans and animals has been associated with the presence of the endosymbiont Sodalis glossinidius. However, intrinsic biological characteristics of the flies and environmental factors can influence the presence of both S. glossinidius and the parasites. It thus remains unclear whether it is the S. glossinidius or other attributes of the flies that explains the apparent association. The objective of this study was to test whether the presence of Trypanosoma vivax, T. congolense and T. brucei are related to the presence of S. glossinidius in tsetse flies when other factors are accounted for: geographic location, species of Glossina, sex or age of the host flies.

Results: Flies (n = 1090) were trapped from four sites in the Shimba Hills and Nguruman regions in Kenya. Sex and species of tsetse (G. austeni, G. brevipalpis, G. longipennis and G. pallidipes) were determined based on external morphological characters and age was estimated by a wing fray score method. The presence of trypanosomes and S. glossinidius was detected using PCR targeting the internal transcribed spacer region 1 and the haemolysin gene, respectively. Sequencing was used to confirm species identification. Generalised Linear Models (GLMs) and Multiple Correspondence Analysis (MCA) were applied to investigate multivariable associations. The overall prevalence of trypanosomes was 42.1%, but GLMs revealed complex patterns of associations: the presence of S. glossinidius was associated with trypanosome presence but only in interactions with other factors and only in some species of trypanosomes. The strongest association was found for T. congolense, and no association was found for T. vivax. The MCA also suggested only a weak association between the presence of trypanosomes and S. glossinidius. Trypanosome-positive status showed strong associations with sex and age while S. glossinidius-positive status showed a strong association with geographic location and species of fly.

Conclusions: We suggest that previous conclusions about the presence of endosymbionts increasing probability of trypanosome presence in tsetse flies may have been confounded by other factors, such as community composition of the tsetse flies and the specific trypanosomes found in different regions.

Keywords: Glossina austeni; Glossina brevipalpis; Glossina longipennis; Glossina pallidipes; Kenya; Secondary endosymbionts; Trypanosoma brucei; Trypanosoma congolense; Trypanosoma vivax; Vector-pathogen interactions.

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Conflict of interest statement

Author’s information

Please note that the data originally appeared in a PhD thesis published by MCh in 2016, under the name Manun Wongserepipatana.

Ethics approval and consent to participate

Authorisation to conduct field studies and tsetse sampling in protected areas was granted by the Kenya Wildlife Service (permits no KWS/BRM/5001). No vertebrate animals or human subjects were used in this study.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

**Fig. 1**
Prevalence of trypanosomes in male (blue) and female (red) tsetse flies with different ages in seven subpopulations. Prevalence in young, juvenile and old flies for (a) *Trypanosoma spp*., (b) *T. vivax*, (c) *T. congolense* and (d) *T. brucei*. BRGp: *G. pallidipes* from Buffalo Ridge; BRGb: *G. brevipalpis* from Buffalo Ridge; ZuGp: *G. pallidipes* from Zungu Luka; ZuGa: G. austeni from Zungu Luka; MuGp: *G. pallidipes* from Mukinyo; MuGl: *G. longipennis* from Mukinyo; SaGl: *G. longipennis* from Sampu. 95% CI error bars are represented. Total numbers of tsetse flies in each category are shown at the base of each bar

**Fig. 2**
Prevalence of *S. glossinidius* in male (blue) and female (red) tsetse flies with different ages in seven subpopulations. Prevalence in young, juvenile and old flies. BRGp: *G. pallidipes* from Buffalo Ridge; BRGb: *G. brevipalpis* from Buffalo Ridge; ZuGp: *G. pallidipes* from Zungu Luka; ZuGa: G. austeni from Zungu Luka; MuGp: *G. pallidipes* from Mukinyo; MuGl: *G. longipennis* from Mukinyo; SaGl: *G. longipennis* from Sampu. 95% CI error bars are represented. Total numbers of tsetse flies in each category are shown at the base of each bar

**Fig. 3**
Comparison of *Trypanosoma* spp. and *S. glossinidius* screening results in tsetse flies. Histograms indicate the percentage of *S. glossinidius*-positive flies for: a) all tsetse flies (N = 1090 samples); b) the Shimba Hills National Reserve (N = 707 samples); and c) Nguruman (N = 383 samples)

**Fig. 4**
Dimensions 1 and 2 of the Multiple Correspondence Analysis 2 showing the relationships among infections of each of the three main species of trypanosomes in relation to *S. glossinidius* status and biological traits of tsetse flies. Sex (male and female), age (young, juvenile and old) and *S. glossinidius* status of the seven subpopulations were plotted for describing associations with the trypanosome status (for each of the three main species of trypanosomes) of tsetse flies. TV: *T. vivax*; TB: *T. brucei*; TC: *T. congolense*. BRGp: *G. pallidipes* from Buffalo Ridge; BRGb: *G. brevipalpis* from Buffalo Ridge; ZuGp: *G. pallidipes* from Zungu Luka; ZuGa: *G. austeni* from Zungu Luka; MuGp: *G. pallidipes* from Mukinyo; MuGl: *G. longipennis* from Mukinyo; SaGl: *G. longipennis* from Sampu

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References

1. Kristjanson PM, Swallow BM, Rowlands GJ, Kruska RL, de Leeuw PN. Measuring the costs of African animal trypanosomosis, the potential benefits of control and returns to research. Agric Syst. 1999;59(1):79–98. doi: 10.1016/S0308-521X(98)00086-9. - DOI
1. Angara T-EE, Ismail AA, Ibrahim AM. An overview on the economic impacts of animal trypanosomiasis. Global J Res Anal. 2014;3(7):275–276. doi: 10.15373/22778160/July2014/99. - DOI
1. Shaw AP. Assessing the economics of animal trypanosomosis in Africa - history and current perspectives. Onderstepoort J Vet Res. 2009;76(1):27–32. doi: 10.4102/ojvr.v76i1.57. - DOI - PubMed
1. Wilson SG, Morris KR, Lewis IJ, Krog E. The effects of trypanosomiasis on rural economy with special reference to the Sudan, Bechuanaland and West Africa. Bull WHO. 1963;28(5–6):595–613. - PMC - PubMed
1. Delespaux V, Geysen D, Van den Bossche P, Geerts S. Molecular tools for the rapid detection of drug resistance in animal trypanosomes. Trends Parasitol. 2008;24(5):236–242. doi: 10.1016/j.pt.2008.02.006. - DOI - PubMed

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[1] Kristjanson PM, Swallow BM, Rowlands GJ, Kruska RL, de Leeuw PN. Measuring the costs of African animal trypanosomosis, the potential benefits of control and returns to research. Agric Syst. 1999;59(1):79–98. doi: 10.1016/S0308-521X(98)00086-9. - DOI

[2] Kristjanson PM, Swallow BM, Rowlands GJ, Kruska RL, de Leeuw PN. Measuring the costs of African animal trypanosomosis, the potential benefits of control and returns to research. Agric Syst. 1999;59(1):79–98. doi: 10.1016/S0308-521X(98)00086-9. - DOI

[3] Angara T-EE, Ismail AA, Ibrahim AM. An overview on the economic impacts of animal trypanosomiasis. Global J Res Anal. 2014;3(7):275–276. doi: 10.15373/22778160/July2014/99. - DOI

[4] Angara T-EE, Ismail AA, Ibrahim AM. An overview on the economic impacts of animal trypanosomiasis. Global J Res Anal. 2014;3(7):275–276. doi: 10.15373/22778160/July2014/99. - DOI

[5] Shaw AP. Assessing the economics of animal trypanosomosis in Africa - history and current perspectives. Onderstepoort J Vet Res. 2009;76(1):27–32. doi: 10.4102/ojvr.v76i1.57. - DOI - PubMed

[6] Shaw AP. Assessing the economics of animal trypanosomosis in Africa - history and current perspectives. Onderstepoort J Vet Res. 2009;76(1):27–32. doi: 10.4102/ojvr.v76i1.57. - DOI - PubMed

[7] Wilson SG, Morris KR, Lewis IJ, Krog E. The effects of trypanosomiasis on rural economy with special reference to the Sudan, Bechuanaland and West Africa. Bull WHO. 1963;28(5–6):595–613. - PMC - PubMed

[8] Wilson SG, Morris KR, Lewis IJ, Krog E. The effects of trypanosomiasis on rural economy with special reference to the Sudan, Bechuanaland and West Africa. Bull WHO. 1963;28(5–6):595–613. - PMC - PubMed

[9] Delespaux V, Geysen D, Van den Bossche P, Geerts S. Molecular tools for the rapid detection of drug resistance in animal trypanosomes. Trends Parasitol. 2008;24(5):236–242. doi: 10.1016/j.pt.2008.02.006. - DOI - PubMed

[10] Delespaux V, Geysen D, Van den Bossche P, Geerts S. Molecular tools for the rapid detection of drug resistance in animal trypanosomes. Trends Parasitol. 2008;24(5):236–242. doi: 10.1016/j.pt.2008.02.006. - DOI - PubMed

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