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Characterization of the cecal microbiome composition of Nigerian indigenous chickens

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Abstract

Poultry cecum microbes are dynamic and complex. They play important roles in disease prevention, detoxification of harmful substances, nutrient processing, and ingestion harvesting. It may be possible to increase poultry productivity by better understanding and controlling the microbial population. We analyzed the composition and function of Nigerian hens’ cecal microbiota using high-throughput sequencing methods. Using high-throughput sequencing of the 16S rRNA genes (V1-V9) hypervariable regions, the cecal microbiota of three Nigerian indigenous chicken genotypes (Naked neck, Frizzle, and Normal feather) was described and compared. A total of two phyla were represented among the three genotypes (Firmicutes and Proteobacteria). Microbiological diversity was found in the community, with naked neck having the most evenness, followed by normal feather, which had the least. There were a lot of similarities between the naked neck and frizzle feather chicken groups when it came to genetic diversity between them. For example, the bacterial cecal microbiota of the naked neck chickens was more diverse, with a higher concentration of motility proteins, two-component systems, bacterial secretion systems, and the formation and breakdown of secondary metabolites. More understanding on gut microbiota roles and interactions will help Nigerian poultry farmers improve their methods and give valuable data for the study of bacteria in the chicken gut.

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Data availability

Raw sequence data is available in Sequence Read Archive (SRA) division of GenBank database. Weblink: https://www.ncbi.nlm.nih.gov/sra/PRJNA762664.

Code availability

The codes used are available on request from main author.

References

  • Adenaike AS, Peters SO, Adeleke MA, Fafiolu AO, Takeet MI, Ikeobi CON (2018) Use of discriminant analysis for the evaluation of coccidiosis resistance parameters in chickens raised in hot humid tropical environment. Trop Anim Health Prod 50:1161–1166

  • Amit-Romach E, Sklan D, Uni Z (2004) Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poultry Sci 83:1093–1098

  • Ardui S, Ameur A, Vermeesch JR, Hestand MS (2018) Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics. Nucleic Acids Res 46(5):2159–2168

  • Atansuyi, A. J., Lasore, C. O. and Chineke, C. A. (2017). Growth performance characteristics and linear body measurement o four chicken genotypes raised under intensive management in South-Western Nigeria. Applied Tropical Agriculture, 22(1) 121-127.

    Google Scholar 

  • Danzeisen JL, Kim HB, Isaacson RE, Tu ZJ, Johnson TJ. 2011. Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS ONE. 6:e27949.

    Article  CAS  Google Scholar 

  • Dhariwal, A., Chong, J., Habib, S., King, I., Agellon, LB., and Xia. J. (2017) MicrobiomeAnalyst - a web-based tool for comprechickensive statistical, visual and meta-analysis of microbiome data Nucleic Acids Research 45 W180–188 (DOI: https://doi.org/10.1093/nar/gkx295) .

  • Frank JA, Pan Y, Tooming-Klunderud A, Eijsink VGH, McHardy AC, Nederbragt AJ et al (2016) Improved metagenome assemblies and taxonomic binning using long-read circular 19 consensus sequence data. Sci Rep 6:25373. https://doi.org/10.1038/srep2537328

  • Hasan N, Yang H (2019) Factors affecting the composition of the gut microbiota, and its modulation. Peer J 16:7:e7502. https://doi.org/10.7717/peerj.7502

  • Hermans D, Van Deun K, Martel A, Van Immerseel F, Messens W, Heyndrickx M, et al. 2011. Colonization factors of Campylobacter jejuni in the chicken gut. Vet Res. 42:82.

    Article  Google Scholar 

  • Hird SH, Sánchez C, Carstens BC, Brumfield RT (2015) Comparative gut microbiota of 59 neotropical bird species neotropical bird species. Front Microbiol 6:1403. https://doi.org/10.3389/fmicb.2015.01403

  • Hu, Y.; Wang, L.; Shao, D.; Wang, Q.; Wu, Y.; Han, Y.; Shi, S. 2020. Selective and Reshape Early Dominant Microbial Community in the Cecum with Similar Proportions and Better Homogenization and Species Diversity Due to Organic Acids as AGP Alternatives Mediate Their Effects on Broilers Growth. Front. Microbiol. 10, 2948.

  • Hueck C.J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev. 62,379–433.

    Article  CAS  Google Scholar 

  • Ikeobi CON, Ozoje MO, Adebambo OA, Adenowo JA, Osinowo OA (1996) Genetic differences in the performance of local chicken in South Western Nigeria. Nig J Genet 9:33–39

  • Ikpeme, E. V., Ekerette, E. E., Efienokwu, J. N. and Ozoje, M. O. (2019). Immune response of Nigeria chicken genotype to salmonella and Newcastle vaccine. Trends in Applied Sciences Research. 121; 296 - 302

    Google Scholar 

  • Iqbal M, Philbin VJ, Withanage GSK, Wigley P, Beal RK, Goodchild MJ, et al. 2005. Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with salmonella enterica serovar typhimurium. Infect Immun. 73, 2344–2350.

    Article  CAS  Google Scholar 

  • Jandhyala SM, Talukdar R, Subramanyam C et al (2015) Role of the normal gut microbiota. World J Gastroenterol 21:8787–803. https://doi.org/10.3748/wjg.v21.i29.8787

  • Kaakoush N, Sodhi N, Chenu J, Cox J, Riordan S, Mitchell H (2014) The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens. Gut Pathogens 6:18

    Article  Google Scholar 

  • Kang, K.; Hu, Y.; Wu, S. Shi, S. 2021. Comparative Metagenomic Analysis of Chicken Gut Microbial Community, Function, and Resistome to Evaluate Noninvasive and Cecal Sampling Resources. Animals 11, 1718. 10.3390/ ani11061718.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kogut MH, Chiang H, Swaggerty CL, Igal Y, Pevzner IY, Huaijun Zhou H (2012) Gene expression analysis of Toll-like receptor pathways in heterophils from genetic chicken lines that differ in their susceptibility to Salmonella enteritidis. Front Genet. https://doi.org/10.3389/fgene.2012.00121

  • Kozik, A.J.; Nakatsu, C.H.; Chun, H.; Jones-Hall, Y.L. 2019. Comparison of the fecal, cecal, and mucus microbiome in male and female mice after TNBS-induced colitis. PLoS ONE, 14, e225079.

    Article  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 31 (9), 814–https://doi.org/10.1038/nbt.2676 WOS:000324306300021. PMID: 23975157

  • Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. 2008. Evolution of mammals and their gut microbes. Science. 320(5883):1647–1651. https://doi.org/10.1126/science.1155725 PMID: 18497261; PubMed Central PMCID: PMC2649005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP, Stedtfeld RD, et al. 2012. In-feed antibiotic effects on the swine intestinal microbiome. P Natl Acad Sci USA. 109(5), 1691–1696. https://doi.org/10.1073/pnas. 1120238109 WOS:000299731400069. PMID: 22307632

    Article  CAS  Google Scholar 

  • Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. 2011. UniFrac: an effective distance metric for microbial community comparison. Isme J. 5(2), 169–172. https://doi.org/10.1038/ismej.2010.133 PMID: 20827291; PubMed Central PMCID: PMC3105689.

    Article  PubMed  Google Scholar 

  • Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD. 2003. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol. 69:6816–24.

    Article  CAS  Google Scholar 

  • Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, Tachibana M, Lorincz MC, Shinkai Y (2010) Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET Nature 464(7290):927–931. https://doi.org/10.1038/nature08858

  • McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. 2012. An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6(3), 610–618.

    Article  CAS  Google Scholar 

  • Mikkelsen H, Sivaneson M, Filloux A. 2011. Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ Microbiol. 13, 1666–1681.

    Article  CAS  Google Scholar 

  • Miska KB, Fetterer RH, Wong EA. 2014. The mRNA expression of amino acid transporters, aminopeptidase N, and the di- and tri-peptide transporter PepT1 in the embryo of the domesticated chicken (Gallus gallus) shows developmental regulation. Poult Sci. 93, 2262–2270.

    Article  CAS  Google Scholar 

  • Moon C, Young W., Maclean P, Cookson A, Bermingham E, 2018. Metagenomic insights into the roles of Proteobacteria in the gastrointestinal microbiomes of healthy dogs and cats. MicrobiologyOpen 7:677.

    Article  Google Scholar 

  • Mohd Shaufi, M.A., Sieo, C.C., Chong, C.W., Gan, H.M. and Ho, Y.W. 2015. Deciphering chicken gut microbial dynamics based on high-throughput 16S rRNA metagenomics analyses. Gut Pathogens 7:4-16 DOI https://doi.org/10.1186/s13099-015-0051-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan E, Campbell JD, Rowe SC, Bispham J, Stevens MP, Bowen AJ, et al. 2004. Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol. 54:994–1010.

    Article  CAS  Google Scholar 

  • Nicholls SM, Quick JC, Tang S, Loman NJ (2019) Ultra-deep, long-read nanopore sequencing of mock microbial community standards. Gigascience 8(5). https://doi.org/10.1093/gigascience/giz04329

  • Oakley, B.B.; Kogut, M.H. 2016. Spatial and temporal changes in the broiler chicken cecal and fecal microbiomes and correlations of bacterial taxa with cytokine gene expression. Front. Vet. Sci., 3, 11.

    Article  Google Scholar 

  • Ocejo M, Oporto B, Hurtado A. 2019. 16S rRNA amplicon sequencing characterization of caecal microbiome composition of broilers and free-range slow-growing chickens throughout their productive lifespan. Sci Rep. 9(1), 2506. https://doi.org/10.1038/s41598-019-39323-x PMID: 30792439; PubMed Central PMCID: PMC6385345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao J, Abe F, Ro Osawa R (2016) Age-related changes in gut microbiota composition from newborn to centenarian: a crosssectional study. BMC Microbio 16(90)

  • Ruiu L (2013) Brevibacillus laterosporus, a Pathogen of Invertebrates and a Broad-Spectrum Antimicrobial Species. Insects 4(3):476–492. https://doi.org/10.3390/insects4030476

  • Pearman W, Smith ANH, Breckell G, Dale J, Freed NE, Silander OK (2018) New tools for diet analyses: nanopore sequencing of metagenomic DNA from stomach contents to quantify diet in an invasive population of rats. bioRxiv. p. 363622. https://www.biorxiv.org/content/early/2018/07/06/363622

  • Polansky O, Sekelova Z, Faldynova M, Sebkova A, Sisak F, Rychlik I. 2016. Important Metabolic Pathways and Biological Processes Expressed by Chicken Cecal Microbiota. Applied and environmental microbi- ology. 82(5):1569–76. https://doi.org/10.1128/Aem.03473-15 WOS:000373338800021. PMID: 26712550

    Article  CAS  Google Scholar 

  • Qu A, Brulc J, Wilson M, Law B, Theoret J, Joens L, et al. 2008. Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS One. 3:e2945.

    Article  Google Scholar 

  • Schloss PD, Handelsman J (2006) Metagenomics for studying unculturable microorganism: cutting the Gordian knot. Genome Biol 6(8):229

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. 2011. Metagenomic biomarker dis- covery and explanation. Genome biology. 12(6), R60. https://doi.org/10.1186/gb-2011-12-6-r60 PMID: 21702898; PubMed Central PMCID: PMC3218848.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shu, B.; Zhang, J.; Sethuraman, V.; Cui, G.; Yi, X.; Zhong, G. 2017. Transcriptome analysis of Spodoptera frugiperda Sf9 cells reveals putative apoptosis-related genes and a preliminary apoptosis mechanism induced by azadirachtin. Sci. Rep. 7, 1–13.

    Article  Google Scholar 

  • Singh R, Dhawan S, Singh K, Kaur J (2012) Cloning, expression and characterization of a metagenome derived thermoactive/thermostable pectinase. Mol Biol Rep 39:8353–8361

  • Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microbiol 77:1153–1161

  • Simpson E (1949) Measurement of diversity. Nature 163:688. https://doi.org/10.1038/163688a0

  • Stanley D, Hughes RJ, Moore RJ. 2014. Microbiota of the chicken gastrointestinal tract: influence on health, productivity and disease. Appl Microbiol Biotechnol. 98:4301–4310.

    Article  CAS  Google Scholar 

  • Tan Z, Luo L, Wang X, Wen Q, Zhou L, Wu K, 2019 Characterization of the cecal microbiome composition of Wenchang chickens before and after fattening. PLoS ONE 14(12): e0225692. https://doi.org/10.1371/journal. Pone.0225692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang KY, Wang ZW, Wan QH, Fang SG (2019) Metagenomics reveals seasonal functional adaptation of the gut microbiome to host feeding and fasting in the Chinese Alligator. Front Microbiol 10:2409. https://doi.org/10.3389/fmicb.2019.02409

  • Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G (2011) Environmental, and gut Bacteroidetes: The Food Connection. Front Microbiol 2:93. https://doi.org/10.3389/fmicb.2011.00093

  • Videnska, P.; Rahman, M.M.; Faldynova, M.; Babak, V.; Matulova, M.E.; Prukner-Radovcic, E.; Krizek, I.; Smole-Mozina, S.; Kovac, J.; Szmolka, A.; et al. 2014. Characterization of egg laying hen and broiler fecal microbiota in poultry farms in Croatia, Czech Republic, Hungary and Slovenia. PLoS ONE 9, e110076.

    Article  Google Scholar 

  • Wei S, Morrison M, Yu Z. 2013. Bacterial census of poultry intestinal microbiome. Poult Sci. 92:671–683.

    Article  CAS  Google Scholar 

  • Wen, C.; Yan, W.; Sun, C.; Ji, C.; Zhou, Q.; Zhang, D.; Zheng, J.; Yang, N. 2019. The gut microbiota is largely independent of host genetics in regulating fat deposition in chickens. ISME J. 13, 1422–1436.

    Article  CAS  Google Scholar 

  • Wick R, Judd LM, Holt KE (2018) Comparison of Oxford nanopore basecalling tools. https://zenodo.org/record/118846930

  • Wosten MM, van Dijk L, Parker CT, Guilhabert MR, van der Meer-Janssen YP, Wagenaar JA, et al. 2010. Growth phase-dependent activation of the DccRS regulon of Campylobacter jejuni. J Bacteriol. 192:2729–2736.

    Article  Google Scholar 

  • Xu Y, Yang H, Zhang L, Su Y, Shi D, Xiao H, et al. 2016. High-throughput sequencing technology to reveal the composition and function of cecal microbiota in Dagu chicken. Bmc Microbiol. 16(1):259. https://doi.org/10.1186/s12866-016-0877-2 PMID: 27814685; PubMed Central PMCID: PMC5097418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan, W.; Sun, C.; Zheng, J.; Wen, C.; Ji, C.; Zhang, D.; Chen, Y.; Hou, Z.; Yang, N. 2019. Efficacy of Fecal Sampling as a Gut Proxy in the Study of Chicken Gut Microbiota. Front. Microbiol. 10: 21-26.

    Article  Google Scholar 

  • Yausheva, E.; Miroshnikov, S.; Sizova, E. 2018. Intestinal microbiome of broiler chickens after use of nanoparticles and metal salts. Environ Sci Pollut Res 25:18109–18120

    Article  CAS  Google Scholar 

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AAS, AU, and ICON designed the work. AAS, AOO, and OO did the statistical analysis. AAS, AU, AOO, OO, AAO, AM, and ICON were involved in writing the manuscript. All the authors read and approved the final manuscript.

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Correspondence to A. S. Adenaike.

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Adenaike, A.S., Akpan, U., Awopejo, O.O. et al. Characterization of the cecal microbiome composition of Nigerian indigenous chickens. Trop Anim Health Prod 54, 211 (2022). https://doi.org/10.1007/s11250-022-03191-x

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