Analysis of Gut Microbiota and Assessment of Environmental Health in Western Anatolian Vole (Microtus lydius Blackler, 1916)
Yıl 2025,
Cilt: 10 Sayı: 4, 471 - 477, 31.07.2025
Tuba Yağcı
,
Gözde Ayseçkin
Öz
The significant risk posed by zoonotic pathogens to humans increases the need to better understand how these pathogens are maintained and transmitted within ecosystems. Microtus (voles), one of the important members of wildlife, are widely distributed in agricultural fields and can directly interact with humans through farmers or agricultural products. Microbiological studies on this genus have identified certain pathogenic bacteria. However, the microbiota of free-living voles in nature also includes members with significant probiotic effects. In this study, the gut microbiota of Microtus lydius, a species widely distributed in Western Anatolia, was characterized for the first time through DNA isolation from fecal samples and the use of 16S rRNA next-generation sequencing technology. The detected bacterial groups were examined across all taxonomic categories. According to the microbial analysis results of the species, the dominant bacteria in the gut microbiota are probiotic in nature, reflecting the species' dietary characteristics. Pathogenic bacteria, on the other hand, are present at low abundance and contribute to species diversity. The microbial records identified for Microtus lydius provide valuable insights for assessing the infectious risks of this species, which interacts with humans in the wild, as well as for understanding the probiotic health effects in social behavior models and contributing to phylogenetic research.
Etik Beyan
Ethical approval is not required.
Destekleyen Kurum
2209-A Tübitak
Proje Numarası
1919B012105702
Teşekkür
This research was supported by TÜBİTAK 2209-A.
Kaynakça
-
Amato, K.R., Jeyakumar, T., Poinar, H., & Gros, P.
(2019). Shifting climates, foods, and diseases: the
human microbiome through evolution. Bioessays,
41(10), 1900034. DOI: 10.1002/bies.201900034
-
Anwar, H., Iftikhar, A., Muzaffar, H., Almatroudi, A.,
Allemailem, K.S., Navaid, S., … & Khurshid,
M. (2021). Biodiversity of gut microbiota: impact
of various host and environmental factors.
BioMed Research International, 2021(1),
5575245. DOI: 10.1155/2021/5575245
-
Assefa, S., Ahles, K., Bigelow, S., Curtis, J.T., & Köhler,
G.A. (2015). Lactobacilli with probiotic potential
in the prairie vole (Microtus ochrogaster). Gut
Pathogens, 7(1), 35. DOI: 10.1186/s13099-015-
0082-0
-
Barnett, T.C., Cole, J.N., Rivera‐Hernandez, T.,
Henningham, A., Paton, J.C., Nizet, V., &
Walker, M.J. (2015). Streptococcal toxins: role
in pathogenesis and disease. Cellular
microbiology, 17(12), 1721-1741. DOI:
10.1111/cmi.12531
-
Bhat, M.I., & Kapila, R. (2017). Dietary metabolites
derived from gut microbiota: critical modulators
of epigenetic changes in mammals. Nutrition
reviews, 75(5), 374-389. DOI:
10.1093/nutrit/nux001
-
Blackler, W.G. (1916). L.-On a new species of Microtus
from Asia Minor. Annals and Magazine of
Natural History, 17(102), 426-427. DOI:
10.1080/00222931608693808
-
Choi, K.J., Yoon, M.Y., Kim, J.-E., & Yoon, S.S. (2023).
Gut commensal Kineothrix alysoides mitigates
liver dysfunction by restoring lipid metabolism
and gut microbial balance. Scientific Reports,
13(1), 14668. DOI: 10.1038/s41598-023-41160-y
-
Curtis, J.T., Assefa, S., Francis, A., & Köhler, G.A.
(2018). Fecal microbiota in the female prairie vole
(Microtus ochrogaster). PLoS One, 13(3),
e0190648. DOI: 10.1371/journal.pone.0190648
-
Flemer, B., Gaci, N., Borrel, G., Sanderson, I.R.,
Chaudhary, P.P., Tottey, W., … & Brugère, J.-
F. (2017). Fecal microbiota variation across the
lifespan of the healthy laboratory rat. Gut
microbes, 8(5), 428-439. DOI:
10.1080/19490976.2017.1334033
-
Gurbanov, R., Kabaoğlu, U., & Yağcı, T. (2022).
Metagenomic analysis of intestinal microbiota in
wild rats living in urban and rural habitats. Folia
Microbiologica, 67(3), 469-477. DOI:
10.1007/s12223-022-00951-y
-
He, W.-q., Xiong, Y.-q., Ge, J., Chen, Y.-x., Chen, X.-j.,
Zhong, X.-s., ... & Mo, Y. (2020). Composition
of gut and oropharynx bacterial communities in
Rattus norvegicus and Suncus murinus in China.
BMC Veterinary Research, 16(1), 413. DOI:
10.1186/s12917-020-02619-6
-
Herrero-Cófreces, S., Mougeot, F., Lambin, X., &
Luque-Larena, J.J. (2021). Linking zoonosis
emergence to farmland invasion by fluctuating
herbivores: common vole populations and
tularemia outbreaks in NW Spain. Frontiers in
Veterinary Science, 8, 698454. DOI:
10.3389/fvets.2021.698454
-
Jacob, J., Manson, P., Barfknecht, R., & Fredricks, T.
(2014). Common vole (Microtus arvalis) ecology
and management: implications for risk assessment
of plant protection products. Pest management
science, 70(6), 869-878. DOI: 10.1002/ps.3695
-
Kauer, L., Imholt, C., Jacob, J., Berens, C., & Kühn, R.
(2024). Seasonal shifts and land-use impact:
unveiling the gut microbiomes of bank voles
(Myodes glareolus) and common voles (Microtus
arvalis). FEMS Microbiology Ecology, 100(12),
fiae159.
DOI:https://doi.org/10.1093/femsec/fiae159
-
Khalil Aria, A. (2011). Ecology and taxonomic status of
the genus Microtus schrank, 1798 (Mammalia:
Rodentia) in North-West Iran. PhD Thesis,
Ankara University, Ankara, Turkey (in Turkish),
Retrieved from
https://acikbilim.yok.gov.tr/handle/20.500.12812
/47973
-
Knowles, S., Eccles, R., & Baltrūnaitė, L. (2019).
Species identity dominates over environment in
shaping the microbiota of small mammals.
Ecology Letters, 22(5), 826-837.
DOI:https://doi.org/10.1111/ele.13240
-
Koskela, K. A., Kalin-Mänttäri, L., Hemmilä, H.,
Smura, T., Kinnunen, P. M., Niemimaa, J., . . .
Nikkari, S. (2017). Metagenomic evaluation of
bacteria from voles. Vector-Borne and Zoonotic
Diseases, 17(2), 123-133.
DOI:https://doi.org/10.1089/vbz.2016.1969
-
Kovtun, A. S., Averina, O. V., Angelova, I. Y., Yunes,
R. A., Zorkina, Y. A., Morozova, A. Y., . . .
Kostyuk, G. P. (2022). Alterations of the
composition and neurometabolic profile of human
gut microbiota in major depressive disorder.
Biomedicines, 10(9), 2162.
DOI:https://doi.org/10.3390/biomedicines100921
62
-
Kusters, J. G., Van Vliet, A. H., & Kuipers, E. J. (2006).
Pathogenesis of Helicobacter pylori infection.
Clinical microbiology reviews, 19(3), 449-490.
DOI:https://doi.org/10.1128/cmr.00054-05
-
Lee, H.-J., Ham, D.-W., Seo, S.-H., Cha, G.-H., & Shin,
E.-H. (2024). Probiotic-induced changes in
intestinal microbiome inhibits Toxoplasma gondii
infection. Parasites, Hosts and Diseases, 62(4),
408. DOI:https://doi.org/10.3347/PHD.24068
-
Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P.
J., Ramey, R. R., Bircher, J. S., . . . Knight, R.
(2008). Evolution of mammals and their gut
microbes. science, 320(5883), 1647-1651.
DOI:https://10.1126/science.1155725
-
Liu, S., Moon, C. D., Zheng, N., Huws, S., Zhao, S., &
Wang, J. (2022). Opportunities and challenges of
using metagenomic data to bring uncultured
microbes into cultivation. Microbiome, 10(1), 76.
DOI:https://doi.org/10.1186/s40168-022-01272-
5
-
Lleal, M., Sarrabayrouse, G., Willamil, J., Santiago, A.,
Pozuelo, M., & Manichanh, C. (2019). A single
faecal microbiota transplantation modulates the
microbiome and improves clinical manifestations
in a rat model of colitis. EBioMedicine, 48, 630-
641. DOI: 10.1016/j.ebiom.2019.10.002
-
Lombardo, M.P. (2008). Access to mutualistic
endosymbiotic microbes: an underappreciated
benefit of group living. Behavioral Ecology and
Sociobiology, 62(4), 479-497. DOI:
10.1007/s00265-007-0428-9
-
Nelson, T.M., Rogers, T.L., & Brown, M.V. (2013). The
gut bacterial community of mammals from marine
and terrestrial habitats. PLoS One, 8(12), e83655.
DOI: 10.1371/journal.pone.0083655
-
Nie, K., Ma, K., Luo, W., Shen, Z., Yang, Z., Xiao, M.,
…, & Wang, X. (2021). Roseburia intestinalis: a
beneficial gut organism from the discoveries in
genus and species. Frontiers in Cellular and
Infection Microbiology, 11, 757718. DOI:
10.3389/fcimb.2021.757718
-
Nuccio, D.A., Normann, M.C., Zhou, H., Grippo, A.J.,
& Singh, P. (2023). Microbiome and metabolome
variation as indicator of social stress in female
prairie voles. International Journal of Molecular
Sciences, 24(2), 1677. DOI:
10.3390/ijms24021677
-
Ochman, H., Worobey, M., Kuo, C.-H., Ndjango, J.-B.
N., Peeters, M., Hahn, B.H., & Hugenholtz, P.
(2010). Evolutionary relationships of wild
hominids recapitulated by gut microbial
communities. PLoS biology, 8(11), e1000546.
DOI: 10.1371/journal.pbio.1000546
-
Org, E., Mehrabian, M., Parks, B.W., Shipkova, P.,
Liu, X., Drake, T.A., & Lusis, A.J. (2016). Sex
differences and hormonal effects on gut
microbiota composition in mice. Gut microbes,
7(4), 313-322. DOI:
10.1080/19490976.2016.1203502
-
Partrick, K.A., Chassaing, B., Beach, L.Q., McCann,
K.E., Gewirtz, A.T., & Huhman, K.L. (2018).
Acute and repeated exposure to social stress
reduces gut microbiota diversity in Syrian
hamsters. Behavioural brain research, 345, 39-
48. DOI: 10.1016/j.bbr.2018.02.005
-
Pereira, A.C., & Cunha, M.V. (2020). An effective
culturomics approach to study the gut microbiota
of mammals. Research in Microbiology, 171(8),
290-300. DOI: 10.1016/j.resmic.2020.09.001
-
Rodríguez-Pastor, R., Escudero, R., Lambin, X., Vidal,
M. D., Gil, H., Jado, I., … & Mougeot, F.
(2019). Zoonotic pathogens in fluctuating
common vole (Microtus arvalis) populations:
occurrence and dynamics. Parasitology, 146(3),
389-398. DOI: 10.1017/S0031182018001543
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Batı Anadolu Tarla Faresi (Microtus lydius Blackler, 1916)’nde Bağırsak Mikrobiyotası Analizi ve Çevresel Sağlık Değerlendirmesi
Yıl 2025,
Cilt: 10 Sayı: 4, 471 - 477, 31.07.2025
Tuba Yağcı
,
Gözde Ayseçkin
Öz
Zoonotik patojenlerin insanlar için önemli bir risk oluşturması, bu patojenlerin ekosistemlerde nasıl korunduğu ve bulaştığı hakkında daha fazla bilgi edinme gerekliliğini artırmaktadır. Yaban hayatının önemli üyelerinden biri olan Microtus (tarla fareleri), tarlalarda geniş bir yayılışa sahiptir ve doğrudan çiftçilerle veya tarım ürünleri aracılığıyla insanlarla etkileşime girebilmektedir. Bu cinse ait mikrobiyolojik çalışmalarda bazı patojenik bakteriler tespit edilmiştir. Bununla birlikte, doğada serbest yaşayan tarla farelerinin mikrobiyotası, önemli probiyotik etkilere sahip üyeler de içermektedir. Bu araştırmada Batı Anadolu’ da geniş bir yayılışa sahip Microtus lydius türünün bağırsak mikrobiyotası, dışkı örneklerinden DNA izolasyonu yapılarak ve 16S rRNA yeni nesil dizileme tekniği kullanılarak ilk kez karakterize edilmiştir. Tespit edilen bakteri grupları, tüm taksonomik kategorilerde incelenmiştir. Türün mikrobiyal analiz sonuçlarına göre, bağırsak mikrobiyotasındaki baskın bakteriler, türün beslenme özelliklerini yansıtacak şekilde ve probiyotik niteliktedir. Patojenik özellikteki bakteriler ise düşük yoğunlukta ve tür çeşitliliğine katkıda bulunmaktadır. Araştırma verileri, yaban hayatında insanlarla etkileşime giren bu türün enfeksiyonel risk değerlendirmesi, sosyal davranış modellerindeki probiyotik sağlık etkileri ve filogenetik araştırmalar için önemli bir katkı sağlayacak niteliktedir.
Etik Beyan
Etik kurul onayı gerekmemektedir.
Destekleyen Kurum
Tübitak 2209-A
Proje Numarası
1919B012105702
Teşekkür
Bu araştırma, TÜBİTAK 2209-A tarafından desteklenmiştir.
Kaynakça
-
Amato, K.R., Jeyakumar, T., Poinar, H., & Gros, P.
(2019). Shifting climates, foods, and diseases: the
human microbiome through evolution. Bioessays,
41(10), 1900034. DOI: 10.1002/bies.201900034
-
Anwar, H., Iftikhar, A., Muzaffar, H., Almatroudi, A.,
Allemailem, K.S., Navaid, S., … & Khurshid,
M. (2021). Biodiversity of gut microbiota: impact
of various host and environmental factors.
BioMed Research International, 2021(1),
5575245. DOI: 10.1155/2021/5575245
-
Assefa, S., Ahles, K., Bigelow, S., Curtis, J.T., & Köhler,
G.A. (2015). Lactobacilli with probiotic potential
in the prairie vole (Microtus ochrogaster). Gut
Pathogens, 7(1), 35. DOI: 10.1186/s13099-015-
0082-0
-
Barnett, T.C., Cole, J.N., Rivera‐Hernandez, T.,
Henningham, A., Paton, J.C., Nizet, V., &
Walker, M.J. (2015). Streptococcal toxins: role
in pathogenesis and disease. Cellular
microbiology, 17(12), 1721-1741. DOI:
10.1111/cmi.12531
-
Bhat, M.I., & Kapila, R. (2017). Dietary metabolites
derived from gut microbiota: critical modulators
of epigenetic changes in mammals. Nutrition
reviews, 75(5), 374-389. DOI:
10.1093/nutrit/nux001
-
Blackler, W.G. (1916). L.-On a new species of Microtus
from Asia Minor. Annals and Magazine of
Natural History, 17(102), 426-427. DOI:
10.1080/00222931608693808
-
Choi, K.J., Yoon, M.Y., Kim, J.-E., & Yoon, S.S. (2023).
Gut commensal Kineothrix alysoides mitigates
liver dysfunction by restoring lipid metabolism
and gut microbial balance. Scientific Reports,
13(1), 14668. DOI: 10.1038/s41598-023-41160-y
-
Curtis, J.T., Assefa, S., Francis, A., & Köhler, G.A.
(2018). Fecal microbiota in the female prairie vole
(Microtus ochrogaster). PLoS One, 13(3),
e0190648. DOI: 10.1371/journal.pone.0190648
-
Flemer, B., Gaci, N., Borrel, G., Sanderson, I.R.,
Chaudhary, P.P., Tottey, W., … & Brugère, J.-
F. (2017). Fecal microbiota variation across the
lifespan of the healthy laboratory rat. Gut
microbes, 8(5), 428-439. DOI:
10.1080/19490976.2017.1334033
-
Gurbanov, R., Kabaoğlu, U., & Yağcı, T. (2022).
Metagenomic analysis of intestinal microbiota in
wild rats living in urban and rural habitats. Folia
Microbiologica, 67(3), 469-477. DOI:
10.1007/s12223-022-00951-y
-
He, W.-q., Xiong, Y.-q., Ge, J., Chen, Y.-x., Chen, X.-j.,
Zhong, X.-s., ... & Mo, Y. (2020). Composition
of gut and oropharynx bacterial communities in
Rattus norvegicus and Suncus murinus in China.
BMC Veterinary Research, 16(1), 413. DOI:
10.1186/s12917-020-02619-6
-
Herrero-Cófreces, S., Mougeot, F., Lambin, X., &
Luque-Larena, J.J. (2021). Linking zoonosis
emergence to farmland invasion by fluctuating
herbivores: common vole populations and
tularemia outbreaks in NW Spain. Frontiers in
Veterinary Science, 8, 698454. DOI:
10.3389/fvets.2021.698454
-
Jacob, J., Manson, P., Barfknecht, R., & Fredricks, T.
(2014). Common vole (Microtus arvalis) ecology
and management: implications for risk assessment
of plant protection products. Pest management
science, 70(6), 869-878. DOI: 10.1002/ps.3695
-
Kauer, L., Imholt, C., Jacob, J., Berens, C., & Kühn, R.
(2024). Seasonal shifts and land-use impact:
unveiling the gut microbiomes of bank voles
(Myodes glareolus) and common voles (Microtus
arvalis). FEMS Microbiology Ecology, 100(12),
fiae159.
DOI:https://doi.org/10.1093/femsec/fiae159
-
Khalil Aria, A. (2011). Ecology and taxonomic status of
the genus Microtus schrank, 1798 (Mammalia:
Rodentia) in North-West Iran. PhD Thesis,
Ankara University, Ankara, Turkey (in Turkish),
Retrieved from
https://acikbilim.yok.gov.tr/handle/20.500.12812
/47973
-
Knowles, S., Eccles, R., & Baltrūnaitė, L. (2019).
Species identity dominates over environment in
shaping the microbiota of small mammals.
Ecology Letters, 22(5), 826-837.
DOI:https://doi.org/10.1111/ele.13240
-
Koskela, K. A., Kalin-Mänttäri, L., Hemmilä, H.,
Smura, T., Kinnunen, P. M., Niemimaa, J., . . .
Nikkari, S. (2017). Metagenomic evaluation of
bacteria from voles. Vector-Borne and Zoonotic
Diseases, 17(2), 123-133.
DOI:https://doi.org/10.1089/vbz.2016.1969
-
Kovtun, A. S., Averina, O. V., Angelova, I. Y., Yunes,
R. A., Zorkina, Y. A., Morozova, A. Y., . . .
Kostyuk, G. P. (2022). Alterations of the
composition and neurometabolic profile of human
gut microbiota in major depressive disorder.
Biomedicines, 10(9), 2162.
DOI:https://doi.org/10.3390/biomedicines100921
62
-
Kusters, J. G., Van Vliet, A. H., & Kuipers, E. J. (2006).
Pathogenesis of Helicobacter pylori infection.
Clinical microbiology reviews, 19(3), 449-490.
DOI:https://doi.org/10.1128/cmr.00054-05
-
Lee, H.-J., Ham, D.-W., Seo, S.-H., Cha, G.-H., & Shin,
E.-H. (2024). Probiotic-induced changes in
intestinal microbiome inhibits Toxoplasma gondii
infection. Parasites, Hosts and Diseases, 62(4),
408. DOI:https://doi.org/10.3347/PHD.24068
-
Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P.
J., Ramey, R. R., Bircher, J. S., . . . Knight, R.
(2008). Evolution of mammals and their gut
microbes. science, 320(5883), 1647-1651.
DOI:https://10.1126/science.1155725
-
Liu, S., Moon, C. D., Zheng, N., Huws, S., Zhao, S., &
Wang, J. (2022). Opportunities and challenges of
using metagenomic data to bring uncultured
microbes into cultivation. Microbiome, 10(1), 76.
DOI:https://doi.org/10.1186/s40168-022-01272-
5
-
Lleal, M., Sarrabayrouse, G., Willamil, J., Santiago, A.,
Pozuelo, M., & Manichanh, C. (2019). A single
faecal microbiota transplantation modulates the
microbiome and improves clinical manifestations
in a rat model of colitis. EBioMedicine, 48, 630-
641. DOI: 10.1016/j.ebiom.2019.10.002
-
Lombardo, M.P. (2008). Access to mutualistic
endosymbiotic microbes: an underappreciated
benefit of group living. Behavioral Ecology and
Sociobiology, 62(4), 479-497. DOI:
10.1007/s00265-007-0428-9
-
Nelson, T.M., Rogers, T.L., & Brown, M.V. (2013). The
gut bacterial community of mammals from marine
and terrestrial habitats. PLoS One, 8(12), e83655.
DOI: 10.1371/journal.pone.0083655
-
Nie, K., Ma, K., Luo, W., Shen, Z., Yang, Z., Xiao, M.,
…, & Wang, X. (2021). Roseburia intestinalis: a
beneficial gut organism from the discoveries in
genus and species. Frontiers in Cellular and
Infection Microbiology, 11, 757718. DOI:
10.3389/fcimb.2021.757718
-
Nuccio, D.A., Normann, M.C., Zhou, H., Grippo, A.J.,
& Singh, P. (2023). Microbiome and metabolome
variation as indicator of social stress in female
prairie voles. International Journal of Molecular
Sciences, 24(2), 1677. DOI:
10.3390/ijms24021677
-
Ochman, H., Worobey, M., Kuo, C.-H., Ndjango, J.-B.
N., Peeters, M., Hahn, B.H., & Hugenholtz, P.
(2010). Evolutionary relationships of wild
hominids recapitulated by gut microbial
communities. PLoS biology, 8(11), e1000546.
DOI: 10.1371/journal.pbio.1000546
-
Org, E., Mehrabian, M., Parks, B.W., Shipkova, P.,
Liu, X., Drake, T.A., & Lusis, A.J. (2016). Sex
differences and hormonal effects on gut
microbiota composition in mice. Gut microbes,
7(4), 313-322. DOI:
10.1080/19490976.2016.1203502
-
Partrick, K.A., Chassaing, B., Beach, L.Q., McCann,
K.E., Gewirtz, A.T., & Huhman, K.L. (2018).
Acute and repeated exposure to social stress
reduces gut microbiota diversity in Syrian
hamsters. Behavioural brain research, 345, 39-
48. DOI: 10.1016/j.bbr.2018.02.005
-
Pereira, A.C., & Cunha, M.V. (2020). An effective
culturomics approach to study the gut microbiota
of mammals. Research in Microbiology, 171(8),
290-300. DOI: 10.1016/j.resmic.2020.09.001
-
Rodríguez-Pastor, R., Escudero, R., Lambin, X., Vidal,
M. D., Gil, H., Jado, I., … & Mougeot, F.
(2019). Zoonotic pathogens in fluctuating
common vole (Microtus arvalis) populations:
occurrence and dynamics. Parasitology, 146(3),
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