Araştırma Makalesi
Batı Anadolu Tarla Faresi (Microtus lydius Blackler, 1916)’nde Bağırsak Mikrobiyotası Analizi ve Çevresel Sağlık Değerlendirmesi
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.
Anahtar Kelimeler
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), 389-398. DOI: 10.1017/S0031182018001543
- Rothschild, D., Weissbrod, O., Barkan, E., Kurilshikov, A., Korem, T., Zeevi, D., … & Bar, N. (2018). Environment dominates over host genetics in shaping human gut microbiota. Nature, 555(7695), 210-215. DOI: 10.1038/nature25973
- Shah, T., Hou, Y., Jiang, J., Shah, Z., Wang, Y., Li, Q., … & Xia, X. (2023). Comparative analysis of the intestinal microbiome in Rattus norvegicus from different geographies. Frontiers in Microbiology, 14, 1283453. DOI: 10.3389/fmicb.2023.1283453
- Tidwell, J., Fusco, J., Nguyen, M.T.T., Nam, G.H., & Goldenberg, S. (2024). Colonizing the Unlikely: Brachyspira in an Immunocompetent Patient. ACG Case Reports Journal, 11(4), e01338. DOI: 10.14309/crj.0000000000001338
- Valdes, A.M., Walter, J., Segal, E., & Spector, T.D. (2018). Role of the gut microbiota in nutrition and health. Bmj, 361. DOI: 10.1136/bmj.k2179
- Yağcı, T. (2019). Species identification of small mammal fauna in Bilecik province and molecular researches for the protection of gene resources. International Journal of Agricultural and Wildlife Sciences, 5(1), 149-160. DOI: 10.24180/ijaws.478168
- Yang, G., Shi, C., Zhang, S., Liu, Y., Li, Z., Gao, F., … & Li, M. (2020). Characterization of the bacterial microbiota composition and evolution at different intestinal tract in wild pigs (Sus scrofa ussuricus). PeerJ, 8, e9124. DOI: 10.7717/peerj.9124
- Yavuz, M., Öz, M., & Albayrak, I. (2011). Ecological preferences of the Anatolian vole Microtus anatolicus (Rodentia: Cricetidae), an endemic species of the Anatolia. Ekoloji, 20(80). DOI: 10.5053/ekoloji.2011.808
Analysis of Gut Microbiota and Assessment of Environmental Health in Western Anatolian Vole (Microtus lydius Blackler, 1916)
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.
Anahtar Kelimeler
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
- Rothschild, D., Weissbrod, O., Barkan, E., Kurilshikov, A., Korem, T., Zeevi, D., … & Bar, N. (2018). Environment dominates over host genetics in shaping human gut microbiota. Nature, 555(7695), 210-215. DOI: 10.1038/nature25973
- Shah, T., Hou, Y., Jiang, J., Shah, Z., Wang, Y., Li, Q., … & Xia, X. (2023). Comparative analysis of the intestinal microbiome in Rattus norvegicus from different geographies. Frontiers in Microbiology, 14, 1283453. DOI: 10.3389/fmicb.2023.1283453
- Tidwell, J., Fusco, J., Nguyen, M.T.T., Nam, G.H., & Goldenberg, S. (2024). Colonizing the Unlikely: Brachyspira in an Immunocompetent Patient. ACG Case Reports Journal, 11(4), e01338. DOI: 10.14309/crj.0000000000001338
- Valdes, A.M., Walter, J., Segal, E., & Spector, T.D. (2018). Role of the gut microbiota in nutrition and health. Bmj, 361. DOI: 10.1136/bmj.k2179
- Yağcı, T. (2019). Species identification of small mammal fauna in Bilecik province and molecular researches for the protection of gene resources. International Journal of Agricultural and Wildlife Sciences, 5(1), 149-160. DOI: 10.24180/ijaws.478168
- Yang, G., Shi, C., Zhang, S., Liu, Y., Li, Z., Gao, F., … & Li, M. (2020). Characterization of the bacterial microbiota composition and evolution at different intestinal tract in wild pigs (Sus scrofa ussuricus). PeerJ, 8, e9124. DOI: 10.7717/peerj.9124
- Yavuz, M., Öz, M., & Albayrak, I. (2011). Ecological preferences of the Anatolian vole Microtus anatolicus (Rodentia: Cricetidae), an endemic species of the Anatolia. Ekoloji, 20(80). DOI: 10.5053/ekoloji.2011.808
Toplam 39 adet kaynakça vardır.
Ayrıntılar
| Birincil Dil | İngilizce |
|---|---|
| Konular | Ekoloji (Diğer), Omurgalı Biyolojisi, Hayvan Bilimi (Diğer) |
| Bölüm | Makaleler |
| Yazarlar | |
| Proje Numarası | 1919B012105702 |
| Erken Görünüm Tarihi | 22 Temmuz 2025 |
| Yayımlanma Tarihi | |
| Gönderilme Tarihi | 19 Mart 2025 |
| Kabul Tarihi | 7 Temmuz 2025 |
| Yayımlandığı Sayı | Yıl 2025 Cilt: 10 Sayı: 4 |
JAES/AAS-Journal of Anatolian Environmental and Animal Sciences/Anatolian Academic Sciences&Anadolu Çevre ve Hayvancılık Dergisi/Anadolu Akademik Bilimler-AÇEH/AAS