Diversity and Co-Occurrence Pattern Analysis of Cecal and Jejunal Microbiota in Two Rabbit Breeds
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Experimental Design and Sampling
2.2. Blood Biochemical Parameters
2.3. Histological Characteristics
2.4. Electron Microscopic Examination
2.5. DNA Extraction, Library Generation, and Sequencing
2.5.1. Bioinformatics—Sequence Processing
2.5.2. Statistical Analysis Diversity
2.5.3. Co-Abundance Analysis
2.5.4. Microbiota-Body Weight Correlations
2.5.5. Microbial Function Prediction
2.6. Statistical Analysis
3. Results
3.1. Body Weight and Weight Gain
3.2. Blood Biochemical Parameters
3.3. Electron Microscopic Examination
3.4. Microbial Profile
3.5. Comparison between Breeds in Cecum Samples
3.6. Comparison between Breeds in Jejunum Samples
3.7. Comparisons between Organs in NM Breed
3.8. Comparisons between Samples in GF Breed
3.9. Correlation and Co-Abundance Analysis
3.10. Microbiota-Body Weight Correlations
3.11. Microbial Function Prediction
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Martinez-Guryn, K.; Hubert, N.; Frazier, K.; Urlass, S.; Musch, M.W.; Ojeda, P.; Pierre, J.F.; Miyoshi, J.; Sontag, T.J.; Cham, C.M. Small intestine microbiota regulate host digestive and absorptive adaptive responses to dietary lipids. Cell Host Microbe 2018, 23, 458–469.e455. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gaboriau-Routhiau, V.; Cerf-Bensussan, N. Gut microbiota and development of the immune system. Med. Sci. M/S 2016, 32, 961–967. [Google Scholar]
- Allam-Ndoul, B.; Castonguay-Paradis, S.; Veilleux, A. Gut microbiota and intestinal trans-epithelial permeability. Int. J. Mol. Sci. 2020, 21, 6402. [Google Scholar] [CrossRef] [PubMed]
- Bäumler, A.J.; Sperandio, V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature 2016, 535, 85–93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hou, K.; Wu, Z.-X.; Chen, X.-Y.; Wang, J.-Q.; Zhang, D.; Xiao, C.; Zhu, D.; Koya, J.B.; Wei, L.; Li, J. Microbiota in health and diseases. Signal Transduct. Target Ther. 2022, 7, 135. [Google Scholar] [CrossRef] [PubMed]
- Crespo-Piazuelo, D.; Estellé, J.; Revilla, M.; Criado-Mesas, L.; Ramayo-Caldas, Y.; Óvilo, C.; Fernández, A.I.; Ballester, M.; Folch, J.M. Characterization of bacterial microbiota compositions along the intestinal tract in pigs and their interactions and functions. Sci. Rep. 2018, 8, 12727. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Q.; Lan, F.; Li, X.; Yan, W.; Sun, C.; Li, J.; Yang, N.; Wen, C. The spatial and temporal characterization of gut microbiota in broilers. Front. Vet. Sci. 2021, 8, 712226. [Google Scholar] [CrossRef]
- Stewart, H.L.; Pitta, D.; Indugu, N.; Vecchiarelli, B.; Engiles, J.B.; Southwood, L.L. Characterization of the fecal microbiota of healthy horses. Am. J. Vet. Res. 2018, 79, 811–819. [Google Scholar] [CrossRef]
- Wang, J.; Xia, S.; Fan, H.; Shao, J.; Tang, T.; Yang, L.; Sun, W.; Jia, X.; Chen, S.; Lai, S. Microbiomics revealed the disturbance of intestinal balance in rabbits with diarrhea caused by stopping the use of an antibiotic diet. Microorganisms 2022, 10, 841. [Google Scholar] [CrossRef]
- Richards, P.; Fothergill, J.; Bernardeau, M.; Wigley, P. Development of the caecal microbiota in three broiler breeds. Front. Vet. Sci. 2019, 6, 201. [Google Scholar] [CrossRef]
- Salem, S.E.; Maddox, T.W.; Berg, A.; Antczak, P.; Ketley, J.M.; Williams, N.J.; Archer, D.C. Variation in faecal microbiota in a group of horses managed at pasture over a 12-month period. Sci. Rep. 2018, 8, 8510. [Google Scholar] [CrossRef] [Green Version]
- AVMA. Avma Pet Ownership and Demographics Sourcebook: 2017–2018 Edition; AVMA: Schaumburg, IL, USA, 2018. [Google Scholar]
- Cotozzolo, E.; Cremonesi, P.; Curone, G.; Menchetti, L.; Riva, F.; Biscarini, F.; Marongiu, M.L.; Castrica, M.; Castiglioni, B.; Miraglia, D. Characterization of bacterial microbiota composition along the gastrointestinal tract in rabbits. Animals 2020, 11, 31. [Google Scholar] [CrossRef]
- Hu, X.; Wang, F.; Yang, S.; Yuan, X.; Yang, T.; Zhou, Y.; Li, Y. Rabbit microbiota across the whole body revealed by 16s rrna gene amplicon sequencing. BMC Microbiol. 2021, 21, 1–16. [Google Scholar] [CrossRef]
- Kylie, J.; Weese, J.S.; Turner, P.V. Comparison of the fecal microbiota of domestic commercial meat, laboratory, companion, and shelter rabbits (oryctolagus cuniculi). BMC Vet. Res. 2018, 14, 1–15. [Google Scholar] [CrossRef]
- Velasco-Galilea, M.; Piles, M.; Ramayo-Caldas, Y.; Sánchez, J.P. The value of gut microbiota to predict feed efficiency and growth of rabbits under different feeding regimes. Sci. Rep. 2021, 11, 19495. [Google Scholar] [CrossRef]
- Chen, S.-Y.; Deng, F.; Jia, X.; Liu, H.; Zhang, G.-W.; Lai, S.-J. Gut microbiota profiling with differential tolerance against the reduced dietary fibre level in rabbit. Sci. Rep. 2019, 9, 288. [Google Scholar] [CrossRef] [Green Version]
- Agradi, S.; Cremonesi, P.; Menchetti, L.; Balzaretti, C.; Severgnini, M.; Riva, F.; Castiglioni, B.; Draghi, S.; Di Giancamillo, A.; Castrica, M. Bovine colostrum supplementation modulates the intestinal microbial community in rabbits. Animals 2023, 13, 976. [Google Scholar] [CrossRef]
- Curone, G.; Biscarini, F.; Cotozzolo, E.; Menchetti, L.; Dal Bosco, A.; Riva, F.; Cremonesi, P.; Agradi, S.; Mattioli, S.; Castiglioni, B. Could dietary supplementation with different sources of n-3 polyunsaturated fatty acids modify the rabbit gut microbiota? Antibiotics 2022, 11, 227. [Google Scholar] [CrossRef]
- Cremonesi, P.; Curone, G.; Biscarini, F.; Cotozzolo, E.; Menchetti, L.; Riva, F.; Marongiu, M.L.; Castiglioni, B.; Barbato, O.; Munga, A. Dietary supplementation with goji berries (lycium barbarum) modulates the microbiota of digestive tract and caecal metabolites in rabbits. Animals 2022, 12, 121. [Google Scholar] [CrossRef]
- Wang, Q.; Fu, W.; Guo, Y.; Tang, Y.; Du, H.; Wang, M.; Liu, Z.; Li, Q.; An, L.; Tian, J. Drinking warm water improves growth performance and optimizes the gut microbiota in early postweaning rabbits during winter. Animals 2019, 9, 346. [Google Scholar] [CrossRef] [Green Version]
- Combes, S.; Michelland, R.J.; Monteils, V.; Cauquil, L.; Soulié, V.; Tran, N.U.; Gidenne, T.; Fortun-Lamothe, L. Postnatal development of the rabbit caecal microbiota composition and activity. FEMS Microbiol. Ecol. 2011, 77, 680–689. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fang, S.; Chen, X.; Zhou, L.; Wang, C.; Chen, Q.; Lin, R.; Xiao, T.; Gan, Q. Faecal microbiota and functional capacity associated with weaning weight in meat rabbits. Microb. Biotechnol. 2019, 12, 1441–1452. [Google Scholar] [CrossRef] [PubMed]
- Read, T.; Fortun-Lamothe, L.; Pascal, G.; Le Boulch, M.; Cauquil, L.; Gabinaud, B.; Bannelier, C.; Balmisse, E.; Destombes, N.; Bouchez, O. Diversity and co-occurrence pattern analysis of cecal microbiota establishment at the onset of solid feeding in young rabbits. Front. Microbiol. 2019, 10, 973. [Google Scholar] [CrossRef] [PubMed]
- Bennegadi, N.; Gidenne, T.; Licois, D. Impact of fibre deficiency and sanitary status on non-specific enteropathy of the growing rabbit. Anim. Res. 2001, 50, 401–413. [Google Scholar] [CrossRef] [Green Version]
- Abecia, L.; Fondevila, M.; Balcells, J.; Lobley, G.; McEwan, N. The effect of medicated diets and level of feeding on caecal microbiota of lactating rabbit does. J. Appl. Microbiol. 2007, 103, 787–793. [Google Scholar] [CrossRef] [PubMed]
- Zou, F.; Zeng, D.; Wen, B.; Sun, H.; Zhou, Y.; Yang, M.; Peng, Z.; Xu, S.; Wang, H.; Fu, X. Illumina miseq platform analysis caecum bacterial communities of rex rabbits fed with different antibiotics. AMB Express 2016, 6, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Liu, B.; Cui, Y.; Ali, Q.; Zhu, X.; Li, D.; Ma, S.; Wang, Z.; Wang, C.; Shi, Y. Gut microbiota modulate rabbit meat quality in response to dietary fiber. Front Nutr. 2022, 9, 849429. [Google Scholar] [CrossRef]
- Castrica, M.; Menchetti, L.; Agradi, S.; Curone, G.; Vigo, D.; Pastorelli, G.; Di Giancamillo, A.; Modina, S.C.; Riva, F.; Serra, V. Effect of bovine colostrum dietary supplementation on rabbit meat quality. Foods 2022, 11, 3433. [Google Scholar] [CrossRef]
- Menchetti, L.; Brecchia, G.; Branciari, R.; Barbato, O.; Fioretti, B.; Codini, M.; Bellezza, E.; Trabalza-Marinucci, M.; Miraglia, D. The effect of goji berries (lycium barbarum) dietary supplementation on rabbit meat quality. Meat Sci. 2020, 161, 108018. [Google Scholar] [CrossRef]
- Ye, X.; Zhou, L.; Zhang, Y.; Xue, S.; Gan, Q.F.; Fang, S. Effect of host breeds on gut microbiome and serum metabolome in meat rabbits. BMC Vet. Res. 2021, 17, 1–13. [Google Scholar] [CrossRef]
- Alshamy, Z.; Richardson, K.C.; Hunigen, H.; Hafez, H.M.; Plendl, J.; Al Masri, S. Comparison of the gastrointestinal tract of a dual-purpose to a broiler chicken line: A qualitative and quantitative macroscopic and microscopic study. PLoS ONE 2018, 13, e0204921. [Google Scholar] [CrossRef] [Green Version]
- Masella, A.P.; Bartram, A.K.; Truszkowski, J.M.; Brown, D.G.; Neufeld, J.D. Pandaseq: Paired-end assembler for illumina sequences. BMC Bioinform. 2012, 13, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I. Qiime allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335–336. [Google Scholar] [CrossRef] [Green Version]
- Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naive bayesian classifier for rapid assignment of rrna sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261–5267. [Google Scholar] [CrossRef] [Green Version]
- Quast, C.; Pruesse, E.; Yilmaz, P.; Gerken, J.; Schweer, T.; Yarza, P.; Peplies, J.; Glöckner, F.O. The silva ribosomal rna gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2012, 41, D590–D596. [Google Scholar] [CrossRef]
- Claesson, M.J.; Jeffery, I.B.; Conde, S.; Power, S.E.; O’connor, E.M.; Cusack, S.; Harris, H.; Coakley, M.; Lakshminarayanan, B.; O’sullivan, O. Gut microbiota composition correlates with diet and health in the elderly. Nature 2012, 488, 178–184. [Google Scholar] [CrossRef]
- Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13, 2498–2504. [Google Scholar] [CrossRef]
- Aßhauer, K.P.; Wemheuer, B.; Daniel, R.; Meinicke, P. Tax4fun: Predicting functional profiles from metagenomic 16s rrna data. Bioinformatics 2015, 31, 2882–2884. [Google Scholar] [CrossRef] [Green Version]
- Abdel-Kafy, E.-S.; El-Deighadi, A.S.; Shabaan, H.M.; Ali, W.H.; Sabra, Z.E.-A.A.; Farid, A. Genetic evaluation for growth traits in new synthetic rabbit line in egypt. Open J. Agric. Res. 2021, 1, 62–73. [Google Scholar] [CrossRef]
- Abdel-Kafy, E.M.G.I.S.; Benlarbi, M.; Ahmed, S.S.; Badawi, Y.K.; Hassan, N.S. Genetic diversity and phenotype characterization of native rabbitin middle-egypt. J. New Sci. 2016, 16, 1312–1320. [Google Scholar]
- Zigo, F.; Pyskatý, O.; Ondrašovičová, S.; Zigová, M.; Šimek, V.; Supuka, P. Comparison of exterior traits in selected giant and medium rabbit breeds. World Rabbit Sci. 2020, 28, 251–266. [Google Scholar] [CrossRef]
- Abdel-Azeem, A.; Abdel-Azim, A.; Darwish, A.; Omar, E. Haematological and biochemical observations in four pure breeds of rabbits and their crosses under egyptian environmental conditions. World Rabbit Sci. 2010, 18, 103–110. [Google Scholar] [CrossRef] [Green Version]
- Abdel-Hamid, T.M.; Dawod, A. Breed effects on growth performance, blood parameters and the levels of metabolic hormones in rabbits under heat stress in egypt. Zagazig Vet. J. 2020, 48, 284–295. [Google Scholar] [CrossRef]
- Ramakrishnan, S. Textbook of Medical Biochemistry; Orient Blackswan: Hyderabad, India, 2004. [Google Scholar]
- Abdel-Khalek, A.E.; Kalaba, Z.M.; El-Gogary, M.R. Functional, anatomical and histological development of caecum in rabbits. Curr. Res. Poult. Sci. 2011, 1, 54–65. [Google Scholar] [CrossRef] [Green Version]
- Takeuchi, A.I.L.R.; O’Hanley, P.D.; Cantey, J.R.; Lushbaugh, W.B. Scanning and transmission electron microscopic study of escherichia coli 015 (rdec-1) enteric infection in rabbit. Infect. Immun. 1978, 19, 686–694. [Google Scholar]
- Fu, X.; Zeng, B.; Wang, P.; Wang, L.; Wen, B.; Li, Y.; Liu, H.; Bai, S.; Jia, G. Microbiome of total versus live bacteria in the gut of rex rabbits. Front. Microbiol. 2018, 9, 733. [Google Scholar] [CrossRef]
- Xiang, X.-D.; Deng, Z.-C.; Wang, Y.-W.; Sun, H.; Wang, L.; Han, Y.-M.; Wu, Y.-Y.; Liu, J.-G.; Sun, L.-H. Organic acids improve growth performance with potential regulation of redox homeostasis, immunity, and microflora in intestines of weaned piglets. Antioxidants 2021, 10, 1665. [Google Scholar] [CrossRef]
- Xu, C.; Yang, S.; Zhu, L.; Cai, X.; Sheng, Y.; Zhu, S.; Xu, J. Regulation of n-acetyl cysteine on gut redox status and major microbiota in weaned piglets. J. Anim. Sci. 2014, 92, 1504–1511. [Google Scholar] [CrossRef] [Green Version]
- Li, H.; Shang, Z.; Liu, X.; Qiao, Y.; Wang, K.; Qiao, J. Clostridium butyricum alleviates enterotoxigenic escherichia coli k88-induced oxidative damage through regulating the p62-keap1-nrf2 signaling pathway and remodeling the cecal microbial community. Front. Immunol. 2021, 12, 771826. [Google Scholar] [CrossRef]
- Adewole, D.; Akinyemi, F. Gut microbiota dynamics, growth performance, and gut morphology in broiler chickens fed diets varying in energy density with or without bacitracin methylene disalicylate (bmd). Microorganisms 2021, 9, 787. [Google Scholar] [CrossRef]
- Hollister, E.B.; Gao, C.; Versalovic, J. Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology 2014, 146, 1449–1458. [Google Scholar] [CrossRef] [Green Version]
- Venegas, D.P.; De La Fuente, M.K.; Landskron, G.; González, M.J.; Quera, R.; Dijkstra, G.; Harmsen, H.J.; Faber, K.N.; Hermoso, M.A. Short chain fatty acids (scfas)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front. Immunol. 2019, 10, 1486. [Google Scholar] [CrossRef] [Green Version]
- Gosalbes, M.J.; Vázquez-Castellanos, J.F.; Angebault, C.; Woerther, P.-L.; Ruppé, E.; Ferrús, M.L.; Latorre, A.; Andremont, A.; Moya, A. Carriage of enterobacteria producing extended-spectrum β-lactamases and composition of the gut microbiota in an amerindian community. Antimicrob. Agents Chemother. 2016, 60, 507–514. [Google Scholar] [CrossRef] [Green Version]
- Wertz, J.T.; Kim, E.; Breznak, J.A.; Schmidt, T.M.; Rodrigues, J.L. Genomic and physiological characterization of the verrucomicrobia isolate diplosphaera colitermitum gen. Nov., sp. Nov., reveals microaerophily and nitrogen fixation genes. Appl. Environ. Microbiol. 2012, 78, 1544–1555. [Google Scholar] [CrossRef] [Green Version]
- Schneeberger, M.; Everard, A.; Gómez-Valadés, A.G.; Matamoros, S.; Ramírez, S.; Delzenne, N.M.; Gomis, R.; Claret, M.; Cani, P.D. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci. Rep. 2015, 5, 16643. [Google Scholar] [CrossRef] [Green Version]
- Linaje, R.; Coloma, M.; Pérez-Martínez, G.; Zúñiga, M. Characterization of faecal enterococci from rabbits for the selection of probiotic strains. J. Appl. Microbiol. 2004, 96, 761–771. [Google Scholar] [CrossRef]
- Andrejčáková, Z.; Sopková, D.; Vlčková, R.; Hertelyová, Z.; Gancarčíková, S.; Nemcová, R. The application of lactobacillus reuteri ccm 8617 and flaxseed positively improved the health of mice challenged with enterotoxigenic E. coli o149: F4. Probiotics Antimicrob. Proteins 2020, 12, 937–951. [Google Scholar] [CrossRef]
- Velasco-Galilea, M.; Piles, M.; Viñas, M.; Rafel, O.; González-Rodríguez, O.; Guivernau, M.; Sánchez, J.P. Rabbit microbiota changes throughout the intestinal tract. Front. Microbiol. 2018, 9, 2144. [Google Scholar] [CrossRef]
Ingredient | % |
---|---|
Barseem | 31.7 |
Barley | 18.0 |
Corn | 10.0 |
Soybean meal 44% | 11.0 |
Wheat bran | 27.0 |
Limestone | 1.0 |
Di-Calcuim | 0.5 |
Methionine | 0.2 |
Salt | 0.3 |
Premix | 0.3 |
Total | 100 |
Chemical Analysis: | |
Crude protein% | 16.4 |
Crude fiber% | 12.7 |
Digestible energy (Kcal/Kg) | 2403 |
Breed | NM | GF | SEM | p Value | |
---|---|---|---|---|---|
Items | |||||
Body Weigh at Week5 | 542.5 | 490.5 | 30.9 | 0.249 | |
Body Weigh at Week12 | 1093.0 | 1229.0 | 83.7 | 0.265 | |
Daily weight gain (DWG) | 11.2 | 15.0 | 1.5 | 0.048 |
Phylum | NM | GF | Order | NM | GF | Genus | NM | GF | p-Value |
---|---|---|---|---|---|---|---|---|---|
Firmicutes | 54 | 65.4 | Bacillales | 1.0 | 1.7 | Bacillus | 1.0 (3.2) | 1.7 (5.5) | 0.387 |
Lactobacillales | 9.9 | 8.1 | Enterococcus | 1.6 (3.5) | 0.5 (1) | 0.808 | |||
Lactobacillus | 8.3 (23.7) | 7.6 (24.1) | 0.382 | ||||||
Clostridiales | 43.1 | 55.6 | Christensenellaceae R-7 group | 4.9 (4.1) | 6.0 (4.6) | 0.571 | |||
Unclassified Clostridiales vadinBB60 group | 1.1 (3.1) | 0.1 (0.3) | 0.679 | ||||||
uncultured Clostridiales vadinBB60 group | 1.3 (2.4) | 0.7 (1.6) | 0.149 | ||||||
uncultured Eubacteriaceae | 7.1 (6.5) | 7.7 (5) | 0.623 | ||||||
Lachnospiraceae (other) | 2 (1.6) | 1.9 (1.4) | 0.940 | ||||||
Lachnospiraceae NK4A136 group | 1.4 (1.7) | 0.9 (0.9) | 0.597 | ||||||
Ruminiclostridium 5 | 1.2 (1.1) | 0.3 (0.4) | 0.082 | ||||||
Ruminococcaceae (other) | 1.1 (0.8) | 0.8 (0.5) | 0.307 | ||||||
Ruminococcaceae NK4A214 group | 8.5 (6.7) | 12.6 (7.6) | 0.273 | ||||||
Ruminococcaceae UCG-013 | 4.1 (3.9) | 5.3 (2.8) | 0.733 | ||||||
Ruminococcaceae UCG-014 | 4.7 (3.4) | 10.1 (6.7) | 0.064 | ||||||
Ruminococcaceae V9D2013 group | 0.6 (0.9) | 1.9 (4.3) | 1.000 | ||||||
Ruminococcus 1 | 1.2 (2) | 1.0 (1.3) | 0.850 | ||||||
Ruminococcus 2 | 0.5 (0.6) | 1.2 (1.4) | 0.272 | ||||||
Subdoligranulum | 3.4 (3.7) | 5.1 (3.7) | 0.212 | ||||||
Bacteroidetes | 7.2 | 3.5 | Bacteroidales | 7.2 | 3.5 | Bacteroides | 4.5 (9.6) | 0.5 (0.9) | 0.256 |
uncultured Muribaculaceae | 1.7 (3.7) | 2.1 (6.4) | 0.451 | ||||||
Alistipes | 1 (1.4) | 0.9 (1.6) | 0.467 | ||||||
Actinobacteria | 1.6 | 1.6 | Coriobacteriales | 1.6 | 1.6 | Atopobiaceae (other) | 1.6 (1.8) | 1.6 (1.7) | 0.850 |
Patescibacteria | 7.3 | 10.3 | Saccharimonadales | 7.3 | 10.3 | Candidatus Saccharimonas | 7.3 (8.2) | 10.3 (6.3) | 0.406 |
Verrucomicrobia | 3.7 | 5.3 | Verrucomicrobiales | 3.7 | 5.3 | Akkermansia | 3.7 (3.1) | 5.3 (5.6) | 0.820 |
Cyanobacteria | 1.3 | 0.6 | Gastranaerophilales | 1.3 | 0.6 | uncultured Gastranaerophilales | 1.3 (1.3) | 0.6 (0.5) | 0.496 |
Phylum | NM | GF | Order | NM | GF | Genus | NM | GF | p-Value |
---|---|---|---|---|---|---|---|---|---|
Firmicutes | 44 | 40.2 | Lactobacillales | 23 | 12.8 | Enterococcus | 13.7 (21.5) | 8.5 (21.8) | 0.472 |
Lactobacillus | 6.4 (13.9) | 3.1 (4.6) | 0.496 | ||||||
Weissella | 2.9 (9.3) | 1.2 (3.8) | 0.804 | ||||||
Clostridiales | 20.6 | 24.1 | Christensenellaceae R-7 group | 0.2 (0.4) | 1.3 (1.7) | 0.088 | |||
Sarcina | 0 (0) | 1.5 (3.4) | 0.451 | ||||||
uncultured Eubacteriaceae | 5.7 (5.5) | 14 (10.9) | 0.054 | ||||||
Lachnospiraceae (other) | 2.4 (4.5) | 0.6 (0.8) | 0.940 | ||||||
Ruminococcaceae NK4A214 group | 3.3 (3.3) | 2.2 (2.1) | 0.545 | ||||||
Ruminococcaceae UCG-014 | 5.8 (7.9) | 2.1 (2.3) | 0.762 | ||||||
Ruminococcaceae V9D2013 group | 0.1 (0.2) | 1.7 (3.3) | 0.384 | ||||||
Subdoligranulum | 3.1 (8.7) | 0.7 (0.8) | 0.596 | ||||||
Erysipelotrichales | 0.4 | 3.3 | Dubosiella | 0.2 (0.3) | 1.9 (2.8) | 0.116 | |||
Erysipelotrichaceae (other) | 0.2 (0.3) | 1.4 (2.3) | 0.180 | ||||||
Proteobacteria | 19.6 | 24.2 | Enterobacteriales | 19 | 19.1 | Citrobacter | 0.1 (0.1) | 1.8 (5.3) | 0.539 |
Escherichia-Shigella | 18.9 (26.6) | 17.3 (23) | 0.571 | ||||||
Pseudomonadales | 0.6 | 5.1 | Pseudomonas | 0.6 (0.6) | 5.1 (14.2) | 0.791 | |||
Actinobacteria | 1.2 | 3.2 | Coriobacteriales | 0.7 | 2.2 | Atopobiaceae (other) | 0.7 (0.8) | 2.2 (3.4) | 0.450 |
Coriobacteriales | 0.5 | 1 | Eggerthellaceae (other) | 0.5 (0.7) | 1 (1.1) | 0.344 | |||
Bacteroidetes | 2.1 | 0.4 | Bacteroidales | 2.1 | 0.4 | Bacteroides | 2.1 (5.1) | 0.4 (0.4) | 0.064 |
Verrucomicrobia | 2.7 | 2.5 | Verrucomicrobiales | 2.7 | 2.5 | Akkermansia | 2.7 (5.3) | 2.5 (6.5) | 0.910 |
Patescibacteria | 6.6 | 1.9 | Saccharimonadales | 6.6 | 1.9 | Candidatus Saccharimonas | 6.6 (9.7) | 1.9 (1.8) | 0.940 |
Phylum | Cecum | Jejunum | Order | Cecum | Jejunum | Genus | Cecum | Jejunum | p-Value |
---|---|---|---|---|---|---|---|---|---|
Firmicutes | 52.9 | 45.8 | Bacillales | 1 | 0.4 | Bacillus | 1.0 (3.2) | 0.4 (0.7) | 0.146 |
Lactobacillales | 9.9 | 23 | Enterococcus | 1.6 (3.5) | 13.7 (21.5) | 0.022 * | |||
Lactobacillus | 8.3 (23.7) | 6.4 (13.9) | 0.405 | ||||||
Weissella | 0.0 (0.0) | 2.9 (9.3) | 0.871 | ||||||
Clostridiales | 42 | 22.4 | Christensenellaceae R-7 group | 4.9 (4.1) | 0.2 (0.4) | 0.013 | |||
Unclassified Clostridiales vadinBB60 group | 1.1 (3.1) | 0.3 (0.7) | 0.936 | ||||||
uncultured Clostridiales vadinBB60 group | 1.3 (2.4) | 0.2 (0.5) | 0.036 * | ||||||
uncultured Eubacteriaceae | 7.1 (6.5) | 5.7 (5.5) | 0.597 | ||||||
Lachnospiraceae (other) | 2.0 (1.6) | 2.4 (4.5) | 0.173 | ||||||
Lachnospiraceae NK4A136 group | 1.4 (1.7) | 0.1 (0.1) | 0.009 * | ||||||
Ruminiclostridium 5 | 1.2 (1.1) | 0.4 (0.8) | 0.031 * | ||||||
Ruminococcaceae (other) | 1.1 (0.8) | 0.3 (0.4) | 0.017 * | ||||||
Ruminococcaceae NK4A214 group | 8.5 (6.7) | 3.3 (3.3) | 0.076 | ||||||
Ruminococcaceae UCG-013 | 4.1 (3.9) | 0.4 (0.4) | 0.075 | ||||||
Ruminococcaceae UCG-014 | 4.7 (3.4) | 5.8 (7.9) | 0.450 | ||||||
Ruminococcus 1 | 1.2 (2.0) | 0.2 (0.4) | 0.058 | ||||||
Subdoligranulum | 3.4 (3.7) | 3.1 (8.7) | 0.096 | ||||||
Bacteroidetes | 7.2 | 2.4 | Bacteroidales | 7.2 | 2.4 | Bacteroides | 4.5 (9.6) | 2.1 (5.1) | 0.240 |
uncultured Muribaculaceae | 1.7 (3.7) | 0.1 (0.1) | 0.721 | ||||||
Alistipes | 1.0 (1.4) | 0.2 (0.4) | 0.050 * | ||||||
Proteobacteria | 0.1 | 18.9 | Enterobacteriales | 0.1 | 18.9 | Escherichia-Shigella | 0.1 (0.3) | 18.9 (26.6) | 0.011 * |
Patescibacteria | 7.3 | 6.6 | Saccharimonadales | 7.3 | 6.6 | Candidatus Saccharimonas | 7.3 (8.2) | 6.6 (9.7) | 0.880 |
Verrucomicrobia | 3.7 | 2.7 | Verrucomicrobiales | 3.7 | 2.7 | Akkermansia | 3.7 (3.1) | 2.7 (5.3) | 0.307 |
Actinobacteria | 1.6 | 0.7 | Coriobacteriales | 1.6 | 0.7 | Atopobiaceae (other) | 1.6 (1.8) | 0.7 (0.8) | 0.472 |
Cyanobacteria | 1.3 | 0.3 | Gastranaerophilales | 1.3 | 0.3 | uncultured Gastranaerophilales | 1.3 (1.3) | 0.3 (0.4) | 0.103 |
Phylum | Cecum | Jejunum | Order | Cecum | Jejunum | Genus | Cecum | Jejunum | p-Value |
---|---|---|---|---|---|---|---|---|---|
Firmicutes | 61.8 | 41.3 | Bacillales | 1.7 | 0.5 | Bacillus | 1.7 (5.5) | 0.5 (1.4) | 0.002 * |
Lactobacillales | 8.1 | 12.8 | Enterococcus | 0.5 (0.01) | 8.5 (21.8) | 0.032 * | |||
Lactobacillus | 7.6 (24.1) | 3.1 (4.6) | 0.010 * | ||||||
Weissella | 0.0 (0.0) | 1.2 (3.8) | 0.754 | ||||||
Clostridiales | 51.8 | 24.7 | Christensenellaceae R-7 group | 6.0 (4.6) | 1.3 (1.7) | 0.011 * | |||
Sarcina | 0.0 (0.0) | 1.5 (3.4) | 0.035 * | ||||||
uncultured Eubacteriaceae | 7.7 (5.0) | 14 (10.9) | 0.212 | ||||||
Lachnospiraceae (other) | 1.9 (1.4) | 0.6 (0.8) | 0.026 * | ||||||
Ruminococcaceae NK4A214 group | 12.6 (7.6) | 2.2 (2.1) | 0.005 * | ||||||
Ruminococcaceae UCG-013 | 5.3 (2.8) | 0.5 (0.5) | 0.002 * | ||||||
Ruminococcaceae UCG-014 | 10.1 (6.7) | 2.1 (2.3) | 0.009 * | ||||||
Ruminococcaceae V9D2013 group | 1.9 (4.3) | 1.7 (3.3) | 0.940 | ||||||
Ruminococcus 2 | 1.2 (1.4) | 0.1 (0.1) | 0.031 * | ||||||
Subdoligranulum | 5.1 (3.7) | 0.7 (0.8) | 0.006 * | ||||||
Erysipelotrichales | 0.2 | 3.3 | Dubosiella | 0.1 (0.1) | 1.9 (2.8) | 0.031 * | |||
Erysipelotrichaceae (other) | 0.1 (0.2) | 1.4 (2.3) | 0.074 | ||||||
Patescibacteria | 10.3 | 1.9 | Saccharimonadales | 10.3 | 1.9 | Candidatus Saccharimonas | 10.3 (6.3) | 1.9 (1.8) | 0.004 * |
Proteobacteria | 0.8 | 24.2 | Enterobacteriales | 0.8 | 24.2 | Citrobacter | 0.0 (0.0) | 1.8 (5.3) | 0.571 |
Escherichia-Shigella | 0.7 (1.6) | 17.3 (23) | 0.007 * | ||||||
Pseudomonas | 0.1 (0.3) | 5.1 (14.2) | 0.074 | ||||||
Actinobacteria | 2.2 | 3.2 | Coriobacteriales | 2.2 | 3.2 | Atopobiaceae (other) | 1.6 (1.7) | 2.2 (3.4) | 0.821 |
Eggerthellaceae (other) | 0.6 (0.5) | 1 (1.1) | 0.597 | ||||||
Verrucomicrobia | 5.3 | 2.5 | Verrucomicrobiales | 5.3 | 2.5 | Akkermansia | 5.3 (5.6) | 2.5 (6.5) | 0.021 * |
Bacteroidetes | 2.1 | 0.9 | Bacteroidales | 2.1 | 0.9 | uncultured Muribaculaceae | 2.1 (6.4) | 0.9 (2.8) | 0.470 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Abdel-Kafy, E.-S.M.; Kamel, K.I.; Severgnini, M.; Morsy, S.H.A.; Cremonesi, P.; Ghoneim, S.S.; Brecchia, G.; Ali, N.I.; Abdel-Ghafar, Y.Z.; Ali, W.A.H.; et al. Diversity and Co-Occurrence Pattern Analysis of Cecal and Jejunal Microbiota in Two Rabbit Breeds. Animals 2023, 13, 2294. https://doi.org/10.3390/ani13142294
Abdel-Kafy E-SM, Kamel KI, Severgnini M, Morsy SHA, Cremonesi P, Ghoneim SS, Brecchia G, Ali NI, Abdel-Ghafar YZ, Ali WAH, et al. Diversity and Co-Occurrence Pattern Analysis of Cecal and Jejunal Microbiota in Two Rabbit Breeds. Animals. 2023; 13(14):2294. https://doi.org/10.3390/ani13142294
Chicago/Turabian StyleAbdel-Kafy, El-Sayed M., Kamel I. Kamel, Marco Severgnini, Shama H. A. Morsy, Paola Cremonesi, Shereen S. Ghoneim, Gabriele Brecchia, Neama I. Ali, Yasmein Z. Abdel-Ghafar, Wael A. H. Ali, and et al. 2023. "Diversity and Co-Occurrence Pattern Analysis of Cecal and Jejunal Microbiota in Two Rabbit Breeds" Animals 13, no. 14: 2294. https://doi.org/10.3390/ani13142294
APA StyleAbdel-Kafy, E.-S. M., Kamel, K. I., Severgnini, M., Morsy, S. H. A., Cremonesi, P., Ghoneim, S. S., Brecchia, G., Ali, N. I., Abdel-Ghafar, Y. Z., Ali, W. A. H., & Shabaan, H. M. A. (2023). Diversity and Co-Occurrence Pattern Analysis of Cecal and Jejunal Microbiota in Two Rabbit Breeds. Animals, 13(14), 2294. https://doi.org/10.3390/ani13142294