Effects of faecal microbiota transplantation on the growth performance, intestinal microbiota, jejunum morphology and immune function of laying-type chicks
Jing Yu
A # , Yujie Zhou A # , Qiongyi Wen A , Baolin Wang A , Haizhou Gong A , Lingyu Zhu A , Hainan Lan A , Bin Wu B , Wuying Lang C , Xin Zheng A * and Min Wu A *
+ Author Affiliations
- Author Affiliations
A College of Animal Science and Technology, Jilin Agricultural University, Changchun 130118, China.
B Jilin Academy of Agricultural Sciences, Changchun 130124, China.
C College of Biology Pharmacy and Food Engineering, Shangluo University, Beixin Street 10, Shangluo 726000, China.
* Correspondence to: zhengxin@jlau.edu.cn, koo331500@163.com
# These authors contributed equally to this paper
Handling Editor: Shaniko Shini
Animal Production Science 62(4) 321-332 https://doi.org/10.1071/AN21093
Submitted: 17 February 2021 Accepted: 15 November 2021 Published: 14 December 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Recent studies have indicated that the early stage of growth is a critical window for intestinal microbiota manipulation to optimise the immunity and body growth. Faecal microbiota transplantation (FMT) is often used to regulate intestinal microbiota colonisation.
Aims: The aim of this study was to explore the effect of FMT on the growth performance, intestinal microbiota, jejunum morphology and immune function of newly hatched laying-type chicks.
Methods: The chicks (Hy-line Brown) were randomly divided into the control group (CON) and FMT group (FMT), which were treated with sterile saline and faecal microbiota suspension of Hy-line Brown breeder hens on Days 1, 3 and 5 respectively. For each group, there were five replications of 12 birds each for 4 weeks. This study investigated the body weight, tibia length, intestinal microflora, jejunum morphology and immune indexes of the chicks.
Key results: The results showed that the body weight and tibia length of birds in the FMT group were significantly increased at 7, 14 and 21 days of age (P < 0.01). Furthermore, we found that FMT altered the intestinal microbiota community of the birds and improved the richness, evenness, diversity and stability of their intestinal microbiota (P < 0.05). The faecal microbiota of the donor hens and birds that received the transplantation were very similar. The villus height and the ratio of the villus to crypt of the birds in the FMT group were significantly (P < 0.0001) higher than those in the control group. In addition, Spearman’s correlation analysis showed that the villus height of the FMT group showed positive correlation with Bacteroides (P < 0.05), and the villus height and the ratio of the villus to crypt in the FMT group showed positive correlations with Megasphaera (P < 0.05). The birds in the FMT group had no significant difference in intestinal length, immune organ indexes, serum β-defensin and IgA concentrations.
Conclusions: In summary, FMT can promote the early growth performance and jejunum morphology of laying-type chicks and improve the intestinal microbiota. FMT has no significant effect on the immune function of chicks.
Implications: FMT may be a potential method to improve the health of chicks to enhance the poultry industry.
Keywords: 16S rRNA, body weight, faecal microbiota transplantation, intestinal microbiota, jejunum morphology, laying-type chicks, Spearman’s correlation analysis, villus height.
References
Abou Elazab MF, Fukushima Y, Horiuchi H, Matsuda H, Furusawa S (2009) Prolonged suppression of chick humoral immune response by antigen specific maternal antibody. Journal of Veterinary Medical Science 71, 417–424.| Prolonged suppression of chick humoral immune response by antigen specific maternal antibody.Crossref | GoogleScholarGoogle Scholar |
Antushevich H (2020) Fecal microbiota transplantation in disease therapy. Clinica Chimica Acta 503, 90–98.
| Fecal microbiota transplantation in disease therapy.Crossref | GoogleScholarGoogle Scholar |
Baldwin S, Hughes RJ, Hao Van TT, Moore RJ, Stanley D (2018) At-hatch administration of probiotic to chickens can introduce beneficial changes in gut microbiota. PLOS ONE 13, e0194825
| At-hatch administration of probiotic to chickens can introduce beneficial changes in gut microbiota.Crossref | GoogleScholarGoogle Scholar | 29570728PubMed |
Baurhoo B, Phillip L, Ruiz-Feria CA (2007) Effects of purified lignin and mannan oligosaccharides on intestinal integrity and microbial populations in the ceca and litter of broiler chickens. Poultry Science 86, 1070–1078.
| Effects of purified lignin and mannan oligosaccharides on intestinal integrity and microbial populations in the ceca and litter of broiler chickens.Crossref | GoogleScholarGoogle Scholar | 17495075PubMed |
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6, 90
| Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin.Crossref | GoogleScholarGoogle Scholar | 29773078PubMed |
Bolyen E, Rideout JR, Dillon MR, et al. (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852–857.
| Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.Crossref | GoogleScholarGoogle Scholar | 31341288PubMed |
Borda-Molina D, Seifert J, Camarinha-Silva A (2018) Current perspectives of the chicken gastrointestinal tract and its microbiome. Computational and Structural Biotechnology Journal 16, 131–139.
| Current perspectives of the chicken gastrointestinal tract and its microbiome.Crossref | GoogleScholarGoogle Scholar | 30026889PubMed |
Bulik-Sullivan EC, Roy S, Elliott RJ, Kassam Z, Lichtman SN, Carroll IM, Gulati AS (2018) Intestinal microbial and metabolic alterations following successful fecal microbiota transplant for d-lactic acidosis. Journal of Pediatric Gastroenterology and Nutrition 67, 483–487.
| Intestinal microbial and metabolic alterations following successful fecal microbiota transplant for d-lactic acidosis.Crossref | GoogleScholarGoogle Scholar | 29901551PubMed |
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583.
| DADA2: high-resolution sample inference from Illumina amplicon data.Crossref | GoogleScholarGoogle Scholar | 27214047PubMed |
Caro-Quintero A, Ritalahti KM, Cusick KD, Löffler FE, Konstantinidis KT (2012) The chimeric genome of Sphaerochaeta: nonspiral spirochetes that break with the prevalent dogma in spirochete biology. mBio 3, e00025-12
| The chimeric genome of Sphaerochaeta: nonspiral spirochetes that break with the prevalent dogma in spirochete biology.Crossref | GoogleScholarGoogle Scholar | 22589287PubMed |
Cheng CS, Wei HK, Wang P, Yu HC, Zhang XM, Jiang SW, Peng J (2019) Early intervention with faecal microbiota transplantation: an effective means to improve growth performance and the intestinal development of suckling piglets. Animal 13, 533–541.
| Early intervention with faecal microbiota transplantation: an effective means to improve growth performance and the intestinal development of suckling piglets.Crossref | GoogleScholarGoogle Scholar | 29983136PubMed |
Cucco M, Guasco B, Malacarne G, Ottonelli R (2006) Effects of beta-carotene supplementation on chick growth, immune status and behaviour in the grey partridge, Perdix perdix. Behavioural Processes 73, 325–332.
| Effects of beta-carotene supplementation on chick growth, immune status and behaviour in the grey partridge, Perdix perdix.Crossref | GoogleScholarGoogle Scholar | 16963199PubMed |
Diao H, Yan HL, Xiao Y, Yu B, Yu J, He J, Zheng P, Zeng BH, Wei H, Mao XB, Chen DW (2016) Intestinal microbiota could transfer host Gut characteristics from pigs to mice. BMC Microbiology 16, 238
| Intestinal microbiota could transfer host Gut characteristics from pigs to mice.Crossref | GoogleScholarGoogle Scholar | 27729007PubMed |
Feye KM, Baxter MFA, Tellez-Isaias G, Kogut MH, Ricke SC (2020) Influential factors on the composition of the conventionally raised broiler gastrointestinal microbiomes. Poultry Science 99, 653–659.
| Influential factors on the composition of the conventionally raised broiler gastrointestinal microbiomes.Crossref | GoogleScholarGoogle Scholar | 32029151PubMed |
Gao P, Ma C, Sun Z, Wang L, Huang S, Su X, Xu J, Zhang H (2017) Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken. Microbiome 5, 91
| Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken.Crossref | GoogleScholarGoogle Scholar | 28768551PubMed |
Gong HZ, Wu M, Lang WY, Yang M, Wang JH, Wang YQ, Zhang Y, Zheng X (2020) Effects of laying breeder hens dietary β-carotene, curcumin, allicin, and sodium butyrate supplementation on the growth performance, immunity, and jejunum morphology of their offspring chicks. Poultry Science 99, 151–162.
| Effects of laying breeder hens dietary β-carotene, curcumin, allicin, and sodium butyrate supplementation on the growth performance, immunity, and jejunum morphology of their offspring chicks.Crossref | GoogleScholarGoogle Scholar | 32416796PubMed |
Hu J, Ma L, Nie Y, Chen J, Zheng W, Wang X, Xie C, Zheng Z, Wang Z, Yang T, Shi M, Chen L, Hou Q, Niu Y, Xu X, Zhu Y, Zhang Y, Wei H, Yan X (2018) A microbiota-derived bacteriocin targets the host to confer diarrhea resistance in early-weaned piglets. Cell Host Microbe 24, 817–832.e8.
| A microbiota-derived bacteriocin targets the host to confer diarrhea resistance in early-weaned piglets.Crossref | GoogleScholarGoogle Scholar | 30543777PubMed |
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.
| MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.Crossref | GoogleScholarGoogle Scholar | 12136088PubMed |
Kim SM, DeFazio JR, Hyoju SK, Sangani K, Keskey R, Krezalek MA, Khodarev NN, Sangwan N, Christley S, Harris KG, Malik A, Zaborin A, Bouziat R, Ranoa DR, Wiegerinck M, Ernest JD, Shakhsheer BA, Fleming ID, Weichselbaum RR, Antonopoulos DA, Gilbert JA, Barreiro LB, Zaborina O, Jabri B, Alverdy JC (2020) Fecal microbiota transplant rescues mice from human pathogen mediated sepsis by restoring systemic immunity. Nature Communications 11, 2354
| Fecal microbiota transplant rescues mice from human pathogen mediated sepsis by restoring systemic immunity.Crossref | GoogleScholarGoogle Scholar | 32393794PubMed |
Kubasova T, Kollarcikova M, Crhanova M, Karasova D, Cejkova D, Sebkova A, Matiasovicova J, Faldynova M, Pokorna A, Cizek A, Rychlik I (2019) Contact with adult hen affects development of caecal microbiota in newly hatched chicks. PLOS ONE 14, e0212446
| Contact with adult hen affects development of caecal microbiota in newly hatched chicks.Crossref | GoogleScholarGoogle Scholar | 30840648PubMed |
Lang W, Hong P, Li R, Zhang H, Huang Y, Zheng X (2019) Growth performance and intestinal morphology of Hyline chickens fed diets with different diet particle sizes. Journal of Animal Physiology and Animal Nutrition 103, 518–524.
| Growth performance and intestinal morphology of Hyline chickens fed diets with different diet particle sizes.Crossref | GoogleScholarGoogle Scholar | 30597646PubMed |
Li P, Yang S, Zhang X, Huang S, Wang N, Wang M, Long M, He J (2018) Zearalenone changes the diversity and composition of caecum microbiota in weaned rabbit. Biomed Research International 2018, 3623274
| Zearalenone changes the diversity and composition of caecum microbiota in weaned rabbit.Crossref | GoogleScholarGoogle Scholar | 30402473PubMed |
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71, 8228–8235.
| UniFrac: a new phylogenetic method for comparing microbial communities.Crossref | GoogleScholarGoogle Scholar | 16332807PubMed |
Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Applied and Environmental Microbiology 73, 1576–1585.
| Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities.Crossref | GoogleScholarGoogle Scholar | 17220268PubMed |
Mackie RI, Aminov RI, Hu W, Klieve AV, Ouwerkerk D, Sundset MA, Kamagata Y (2003) Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches. Applied and Environmental Microbiology 69, 6808–6815.
| Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches.Crossref | GoogleScholarGoogle Scholar | 14602644PubMed |
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet Journal 17, 10–12
| Cutadapt removes adapter sequences from high-throughput sequencing reads.Crossref | GoogleScholarGoogle Scholar |
Martínez I, Maldonado-Gomez MX, Gomes-Neto Jão C, Kittana H, Ding H, Schmaltz R, Joglekar P, Cardona RJ, Marsteller NL, Kembel SW, Benson AK, Peterson DA, Ramer-Tait AE, Walter J (2018) Experimental evaluation of the importance of colonization history in early-life gut microbiota assembly. Elife 7, e36521
| Experimental evaluation of the importance of colonization history in early-life gut microbiota assembly.Crossref | GoogleScholarGoogle Scholar | 30226190PubMed |
McCormack UM, Curião T, Metzler-Zebeli BU, Wilkinson T, Reyer H, Crispie F, Cotter PD, Creevey CJ, Gardiner GE, Lawlor PG, Dudley EG (2019) Improvement of feed efficiency in pigs through microbial modulation via fecal microbiota transplantation in sows and dietary supplementation of inulin in offspring. Applied and Environmental Microbiology 85, e01255-19
| Improvement of feed efficiency in pigs through microbial modulation via fecal microbiota transplantation in sows and dietary supplementation of inulin in offspring.Crossref | GoogleScholarGoogle Scholar | 31519656PubMed |
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. The ISME Journal 6, 610–618.
| An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea.Crossref | GoogleScholarGoogle Scholar | 22134646PubMed |
Medvecky M, Cejkova D, Polansky O, Karasova D, Kubasova T, Cizek A, Rychlik I (2018) Whole genome sequencing and function prediction of 133 gut anaerobes isolated from chicken caecum in pure cultures. BMC Genomics 19, 561
| Whole genome sequencing and function prediction of 133 gut anaerobes isolated from chicken caecum in pure cultures.Crossref | GoogleScholarGoogle Scholar | 30064352PubMed |
Pluske JR, Turpin DL, Kim J-C (2018) Gastrointestinal tract (gut) health in the young pig. Animal Nutrition 4, 187–196.
| Gastrointestinal tract (gut) health in the young pig.Crossref | GoogleScholarGoogle Scholar | 30140758PubMed |
Price MN, Dehal PS, Arkin AP (2010) FastTree 2 – approximately maximum-likelihood trees for large alignments. PLOS ONE 5, e9490
| FastTree 2 – approximately maximum-likelihood trees for large alignments.Crossref | GoogleScholarGoogle Scholar | 20224823PubMed |
Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiology Ecology 62, 142–160.
| Multivariate analyses in microbial ecology.Crossref | GoogleScholarGoogle Scholar | 17892477PubMed |
Ranjitkar S, Lawley B, Tannock G, Engberg RM (2016) Bacterial succession in the broiler gastrointestinal tract. Applied and Environmental Microbiology 82, 2399–2410.
| Bacterial succession in the broiler gastrointestinal tract.Crossref | GoogleScholarGoogle Scholar | 26873323PubMed |
Rosewarne CP, Cheung JL, Smith WJM, Evans PN, Tomkins NW, Denman SE, Páraic ÓC, Morrison M (2012) Draft genome sequence of Treponema sp. strain JC4, a novel spirochete isolated from the bovine rumen. Journal of Bacteriology 194, 4130
| Draft genome sequence of Treponema sp. strain JC4, a novel spirochete isolated from the bovine rumen.Crossref | GoogleScholarGoogle Scholar | 22815447PubMed |
Rubio LA (2019) Possibilities of early life programming in broiler chickens via intestinal microbiota modulation. Poultry Science 98, 695–706.
| Possibilities of early life programming in broiler chickens via intestinal microbiota modulation.Crossref | GoogleScholarGoogle Scholar | 30247675PubMed |
Schwarzer M, Strigini M, Leulier F (2018) Gut microbiota and host juvenile growth. Calcified Tissue International 102, 387–405.
| Gut microbiota and host juvenile growth.Crossref | GoogleScholarGoogle Scholar | 29214457PubMed |
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biology 12, R60
| Metagenomic biomarker discovery and explanation.Crossref | GoogleScholarGoogle Scholar | 21702898PubMed |
Siegerstetter S-C, Petri Rée M, Magowan E, Lawlor PG, Zebeli Q, O’Connell NE, Metzler-Zebeli BU, Dudley EG (2018) Fecal microbiota transplant from highly feed-efficient donors shows little effect on age-related changes in feed-efficiency-associated fecal microbiota from chickens. Applied and Environmental Microbiology 84, e02330-17
| Fecal microbiota transplant from highly feed-efficient donors shows little effect on age-related changes in feed-efficiency-associated fecal microbiota from chickens.Crossref | GoogleScholarGoogle Scholar | 29101192PubMed |
Van Immerseel F, De Buck J, Pasmans F, Velge P, Bottreau E, Fievez V, Haesebrouck F, Ducatelle R (2003) Invasion of Salmonella enteritidis in avian intestinal epithelial cells in vitro is influenced by short-chain fatty acids. International Journal of Food Microbiology 85, 237–248.
| Invasion of Salmonella enteritidis in avian intestinal epithelial cells in vitro is influenced by short-chain fatty acids.Crossref | GoogleScholarGoogle Scholar | 12878382PubMed |
Vaughn BP, Vatanen T, Allegretti JR, Bai A, Xavier RJ, Korzenik J, Gevers D, Ting A, Robson SC, Moss AC (2016) Increased intestinal microbial diversity following fecal microbiota transplant for active Crohn’s disease. Inflammatory Bowel Diseases 22, 2182–2190.
| Increased intestinal microbial diversity following fecal microbiota transplant for active Crohn’s disease.Crossref | GoogleScholarGoogle Scholar | 27542133PubMed |
Wang L, Lilburn M, Yu Z (2016) Intestinal microbiota of broiler chickens as affected by litter management regimens. Frontiers in Microbiology 7, 593
| Intestinal microbiota of broiler chickens as affected by litter management regimens.Crossref | GoogleScholarGoogle Scholar | 27242676PubMed |
Wang K, Liao M, Zhou N, Bao L, Ma K, Zheng Z, Wang Y, Liu C, Wang W, Wang J, Liu S-J, Liu H (2019) Parabacteroides distasonis alleviates obesity and metabolic dysfunctions via production of succinate and secondary bile acids. Cell Reports 26, 222–235.e5.
| Parabacteroides distasonis alleviates obesity and metabolic dysfunctions via production of succinate and secondary bile acids.Crossref | GoogleScholarGoogle Scholar | 30605678PubMed |
Weingarden A, González A, Vázquez-Baeza Y, Weiss S, Humphry G, Berg-Lyons D, Knights D, Unno T, Bobr A, Kang J, Khoruts A, Knight R, Sadowsky MJ (2015) Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection. Microbiome 3, 10
| Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection.Crossref | GoogleScholarGoogle Scholar | 25825673PubMed |
Yoshikawa S, Araoka R, Kajihara Y, Ito T, Miyamoto H, Kodama H (2018) Valerate production by Megasphaera elsdenii isolated from pig feces. Journal of Bioscience And Bioengineering 125, 519–524.
| Valerate production by Megasphaera elsdenii isolated from pig feces.Crossref | GoogleScholarGoogle Scholar | 29331526PubMed |
