AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (2 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

SMRT sequencing and ddPCR reveal the complexity of developmental trajectories and temporal dynamics of gut bifidobacterial communities in infants

Xu Gao1Tao Zhang1Xiaoye BaiQiannan WenDongyu LiLai-Yu KwokHeping ZhangZhihong Sun( )
Key Laboratory of Dairy Biotechnology and Engineering, Ministry of Education; Key Laboratory of Dairy Products Processing, Ministry of Agriculture and Rural Affairs; Inner Mongolia Key Laboratory of Dairy Biotechnology and Engineering, Inner Mongolia Agricultural University, Hohhot 010018, China

1 These authors contributed equally.

Peer review under responsibility of KeAi Communications Co., Ltd.

Show Author Information

Abstract

Infant intestinal microbiome is closely linked with health and risk of disease. Bifidobacterium are important components of the infant gut and are known to confer various health effects on the host. However, few studies have described the precise composition and dynamics of early infant gut bifidobacterial communities. Thus, this was a pilot study aiming to describe the developmental trajectories and temporal dynamics of bifidobacterial communities in infants before 6 months of age. A total of 28 fecal samples from 4 infants (GF, ZZ, QM, TN, respectively) were collected and analyzed after 5, 15, 30, 60, 90, 120, 150, and 180 days of birth by a bifidobacteria-target method (based on single-molecule real-time sequencing of partial bifidobacterial rpsK genes) in conjunction with droplet digital polymerase chain reaction (ddPCR). The infant fecal microbiota comprised a total of 11 bifidobacterial species, including 4 major species, i.e., B. dentium (37.35%), B. catenulatum (32.04%), B. breve (22.24%), and B. animalis (8.02%). The infant microbiota showed highly individualized developmental trajectories. The leading species for GF was B. catenulatum, with a relatively stable developmental trajectory. In ZZ, B. breve was enriched, and the developmental trajectory was rather fluctuating. The most abundant species for QM and TN was B. dentium. The developmental trajectory of B. dentium in QM showed a trend of gradual decrease, whereas an opposite trend was seen in samples of TN. The results of ddPCR confirmed large variations in quantities of bifidobacteria between infants and suggested discordances in temporal dynamics of bifidobacterial communities during the first half year of infancy. In conclusion, our results suggested that the early infant gut bifidobacterial microbiota was highly complex and temporal dynamics, with individualized developmental trajectories, which should be considered in future research of infant gut microbiota.

References

[1]

J. Libertucci, V.B. Young, The role of the microbiota in infectious diseases, Nat. Microbiol. 4(1) (2019) 35-45. https://doi.org/10.1038/s41564-018-0278-4.

[2]

S.V. Lynch, O. Pedersen, The human intestinal microbiome in health and disease, N. Engl. J. Med. 375(24) (2016) 2369-2379. https://doi.org/10.1056/NEJMra1600266.

[3]

M.E. Perez-Muñoz, M.C. Arrieta, A.E. Ramer-Tait, et al., A critical assessment of the "sterile womb" and "in utero colonization" hypotheses: implications for research on the pioneer infant microbiome, Microbiome 5(1) (2017) 48. https://doi.org/10.1186/s40168-017-0268-4.

[4]

E.S. Lim, Y. Zhou, G. Zhao, et al., Early life dynamics of the human gut virome and bacterial microbiome in infants, Nat. Med. 21(10) (2015) 1228-1234. https://doi.org/10.1038/nm.3950.

[5]

T. Feehley, C.H. Plunkett, R. Bao, et al., Healthy infants harbor intestinal bacteria that protect against food allergy, Nat. Med. 25(3) (2019) 448-453. https://doi.org/10.1038/s41591-018-0324-z.

[6]

M.C. Arrieta, L.T. Stiemsma, P.A. Dimitriu, et al., Early infancy microbial and metabolic alterations affect risk of childhood asthma, Sci. Transl. Med. 7(307) (2015) 307ra152. https://doi.org/10.1126/scitranslmed.aab2271.

[7]

T.R. Abrahamsson, H.E. Jakobsson, A.F. Andersson, et al., Low diversity of the gut microbiota in infants with atopic eczema, J. Allergy Clin. Immunol. 129(2) (2012) 434-440. https://doi.org/10.1016/j.jaci.2011.10.025.

[8]

L.M. Cox, S. Yamanishi, J. Sohn, et al., Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences, Cell 158(4) (2014) 705-721. https://doi.org/10.1016/j.cell.2014.05.052.

[9]

A.D. Kostic, D. Gevers, H. Siljander, et al., The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes, Cell Host Microbe. 17(2) (2015) 260-273. https://doi.org/10.1016/j.chom.2015.01.001.

[10]

J. Torres, J. Hu, A. Seki, et al., Infants born to mothers with IBD present with altered gut microbiome that transfers abnormalities of the adaptive immune system to germ-free mice, Gut 69(1) (2020) 42-51. https://doi.org/10.1136/gutjnl-2018-317855.

[11]

M.C. Arrieta, L.T. Stiemsma, N. Amenyogbe, et al., The intestinal microbiome in early life: health and disease, Front. Immunol. 5 (2014) 427. https://doi.org/10.3389/fimmu.2014.00427.

[12]

F. Turroni, C. Milani, S. Duranti, et al., The infant gut microbiome as a microbial organ influencing host well-being, Ital. J. Pediatr. 46(1) (2020) 16. https://doi.org/10.1186/s13052-020-0781-0.

[13]

F. Bäckhed, J. Roswall, Y. Peng, et al., Dynamics and stabilization of the human gut microbiome during the first year of life, Cell Host Microbe. 17(5) (2015) 690-703. https://doi.org/10.1016/j.chom.2015.04.004.

[14]

C.J. Stewart, N.J. Ajami, J.L. O'Brien, et al., Temporal development of the gut microbiome in early childhood from the TEDDY study, Nature 562(7728) (2018) 583-588. https://doi.org/10.1038/s41586-018-0617-x.

[15]

T. Vatanen, E.A. Franzosa, R. Schwager, et al., The human gut microbiome in early-onset type 1 diabetes from the TEDDY study, Nature 562(7728) (2018) 589-594. https://doi.org/10.1038/s41586-018-0620-2.

[16]

C. Milani, S. Duranti, F. Bottacini, et al., The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota, Microbiol. Mol. Biol. Rev. 81(4) (2017) e00036-17. https://doi.org/10.1128/MMBR.00036-17.

[17]

F. Turroni, C. Milani, S. Duranti, et al., Bifidobacteria and the infant gut: an example of co-evolution and natural selection, Cell Mol. Life Sci. 75(1) (2018) 103-118. https://doi.org/10.1007/s00018-017-2672-0.

[18]

V. Liévin, I. Peiffer, S. Hudault, et al., Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity, Gut 47(5) (2000) 646-652. https://doi.org/10.1136/gut.47.5.646.

[19]

A.W. Walker, J.C. Martin, P. Scott, et al., 16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice, Microbiome 3 (2015) 26. https://doi.org/10.1186/s40168-015-0087-4.

[20]

X.Y. Bai, L.L. Shen, X. Gao, et al., Differential structures and enterotype-like clusters of Bifidobacterium responses to probiotic fermented milk consumption across subjects using a Bifidobacterium-target procedure, Food Res. Int. 140 (2021) 109839. https://doi.org/10.1016/j.foodres.2020.109839.

[21]

C.M. Hindson, J.R. Chevillet, H.A. Briggs, et al., Absolute quantification by droplet digital PCR versus analog real-time PCR, Nat. Methods 10(10) (2013) 1003-1005. https://doi.org/10.1038/nmeth.2633.

[22]

X. Gao, X.Y. Bai, H.J. Zheng, et al., Design and evaluation of Bifidobacterium genus-specific primer for quantification, Acta Microbiologia Sinica. 60(3) (2020) 545-555. https://doi.org/10.13343/j.cnki.wsxb.20190228.

[23]

Q.C. Hou, F.Y. Zhao, W.J. Liu, et al., Probiotic-directed modulation of gut microbiota is basal microbiome dependent, Gut Microbes. 12(1) (2020) 1736974. https://doi.org/10.1080/19490976.2020.1736974.

[24]

M. Tanaka, J. Nakayama, Development of the gut microbiota in infancy and its impact on health in later life, Allergol. Int. 66(4) (2017) 515-522. https://doi.org/10.1016/j.alit.2017.07.010.

[25]

B. Cukrowska, J.B. Bierła, M. Zakrzewska, et al., The relationship between the infant gut microbiota and allergy. the role of Bifidobacterium breve and prebiotic oligosaccharides in the activation of anti-allergic mechanisms in early life, Nutrients 12(4) (2020) 946. https://doi.org/10.3390/nu12040946.

[26]

C. Hidalgo-Cantabrana, S. Delgado, L. Ruiz, et al., Bifidobacteria and their health-promoting effects, Microbiol. Spectr. 5(3) (2017) 73-98. https://doi.org/10.1128/microbiolspec.BAD-0010-2016.

[27]

R. Tojo, A. Suárez, M.G. Clemente, et al., Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis, World J. Gastroenterol. 20(41) (2014) 15163-15176. https://doi.org/10.3748/wjg.v20.i41.15163.

[28]

F. Turroni, C. Peano, D.A. Pass, et al., Diversity of bifidobacteria within the infant gut microbiota, PLoS One 7(5) (2014) e36957. https://doi.org/10.1371/journal.pone.0036957.

[29]

W.L. Yan, B.L. Luo, X.Y. Zhang, et al., Association and occurrence of bifidobacterial phylotypes between breast milk and fecal microbiomes in mother-infant dyads during the first 2 years of life, Front. Microbiol. 12 (2021) 669442. https://doi.org/10.3389/fmicb.2021.669442.

[30]

S. Saturio, A.M. Nogacka, M. Suárez, et al., Early-life development of the bifidobacterial community in the infant gut, Int. J. Mol. Sci. 22(7) (2021) 3382. https://doi.org/10.3390/ijms22073382.

[31]

B. Yang, Y. Chen, C. Stanton, et al., Bifidobacterium and Lactobacillus composition at species level and gut microbiota diversity in infants before 6 weeks, Int. J. Mol. Sci. 20(13) (2019) 3306. https://doi.org/10.3390/ijms20133306.

[32]

B. Lawley, A. Otal, K. Moloney-Geany, et al., Fecal microbiotas of Indonesian and New Zealand children differ in complexity and bifidobacterial taxa during the first year of life, Appl. Environ. Microbiol. 85(19) (2019) e01105- e01119. https://doi.org/10.1128/AEM.01105-19.

[33]

B. Yang, M. Ding, Y. Chen, et al., Development of gut microbiota and bifidobacterial communities of neonates in the first 6 weeks and their inheritance from mother, Gut Microbes. 13(1) (2021) 1-13. https://doi.org/10.1080/19490976.2021.1908100.

[34]

C. Milani, G.A. Lugli, F. Turroni, et al., Evaluation of bifidobacterial community composition in the human gut by means of a targeted amplicon sequencing (ITS) protocol, FEMS Microbiol. Ecol. 90(2) (2014) 493-503. https://doi.org/10.1111/1574-6941.12410.

[35]

Y. Sun, T. Zuo, C.P. Cheung, et al., Population-level configurations of gut mycobiome across 6 ethnicities in urban and rural China, Gastroenterology 160(1) (2021) 272-286. https://doi.org/10.1053/j.gastro.2020.09.014.

[36]

M. Deschasaux, K.E. Bouter, A. Prodan, et al., Depicting the composition of gut microbiota in a population with varied ethnic origins but shared geography, Nat. Med. 24(10) (2018) 1526-1531. https://doi.org/10.1038/s41591-018-0160-1.

[37]

R. Yang, R. Gao, S. Cui, et al., Dynamic signatures of gut microbiota and influences of delivery and feeding modes during the first 6 months of life, Physiol. Genomics. 51(8) (2019) 368-378. https://doi.org/10.1152/physiolgenomics.00026.2019.

[38]

E. Barrett, A.K. Deshpandey, C.A. Ryan, et al., The neonatal gut harbours distinct bifidobacterial strains, Arch. Dis. Child. Fetal Neonatal Ed. 100(5) (2015) 405-410. https://doi.org/10.1136/archdischild-2014-306110.

[39]

M.J. Claesson, I.B. Jeffery, S. Conde, et al., Gut microbiota composition correlates with diet and health in the elderly, Nature 488(7410) (2012) 178-184. https://doi.org/10.1038/nature11319.

[40]

L.A. David, C.F. Maurice, R.N. Carmody, et al., Diet rapidly and reproducibly alters the human gut microbiome, Nature 505(7484) (2014) 559-563. https://doi.org/10.1038/nature12820.

[41]

N. Zmora, J. Suez, E. Elinav, You are what you eat: diet, health and the gut microbiota, Nat. Rev. Gastroenterol. Hepatol. 16(1) (2019) 35-56. https://doi.org/10.1038/s41575-018-0061-2.

[42]

S.N. Lundgren, J.C. Madan, J.A. Emond, et al., Maternal diet during pregnancy is related with the infant fecal microbiome in a delivery mode-dependent manner, Microbiome 6(1) (2018) 109. https://doi.org/10.1186/s40168-018-0490-8.

[43]

E. Rutayisire, K. Huang, Y. Liu, et al., The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants' life: a systematic review, BMC Gastroenterol. 16(1) (2016) 86. https://doi.org/10.1186/s12876-016-0498-0.

[44]

M. Reyman, M.A. van Houten, D. van Baarle, et al., Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life, Nat. Commun. 10(1) (2019) 4997. https://doi.org/10.1038/s41467-019-13014-7.

[45]

F. Fouhy, C. Watkins, C.J. Hill, et al., Perinatal factors affect the gut microbiota up to four years after birth, Nat. Commun. 10(1) (2019) 1517. https://doi.org/10.1038/s41467-019-09252-4.

[46]

J.C. Madan, A.G. Hoen, S.N. Lundgren, et al., Association of cesarean delivery and formula supplementation with the intestinal microbiome of 6-week-old infants, JAMA Pediatr. 170(3) (2016) 212-219. https://doi.org/10.1001/jamapediatrics.2015.3732.

[47]

M. Selma-Royo, M. Calatayud Arroyo, I. García-Mantrana, et al., Perinatal environment shapes microbiota colonization and infant growth: impact on host response and intestinal function, Microbiome 8(1) (2020) 167. https://doi.org/10.1186/s40168-020-00940-8.

[48]

L. Wampach, A. Heintz-Buschart, J.V. Fritz, et al., Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential, Nat. Commun. 9(1) (2018) 5091. https://doi.org/10.1038/s41467-018-07631-x.

[49]

J. Xu, B. Lawley, G. Wong, et al., Ethnic diversity in infant gut microbiota is apparent before the introduction of complementary diets, Gut Microbes. 11(5) (2020) 1362-1373. https://doi.org/10.1080/19490976.2020.1756150.

[50]

J. de la Cuesta-Zuluaga, S.T. Kelley, Y. Chen, et al., Age- and sex-dependent patterns of gut microbial diversity in human adults, mSystems 4(4) (2019) e00261-19. https://doi.org/10.1128/mSystems.00261-19.

[51]

L. Yurkovetskiy, M. Burrows, A.A. Khan, et al., Gender bias in autoimmunity is influenced by microbiota, Immunity 39(2) (2013) 400-412. https://doi.org/10.1016/j.immuni.2013.08.013.

[52]

J.G. Markle, D.N. Frank, S. Mortin-Toth, et al., Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity, Science 339(6123) (2013) 1084-1088. https://doi.org/10.1126/science.1233521.

[53]

J.A. Santos-Marcos, C. Haro, A. Vega-Rojas, et al., Sex differences in the gut microbiota as potential determinants of gender predisposition to disease, Mol. Nutr. Food Res. 63(7) (2019) e1800870. https://doi.org/10.1002/mnfr.201800870.

[54]

T.T.B. Ho, M.W. Groer, B. Kane, et al., Dichotomous development of the gut microbiome in preterm infants, Microbiome 6(1) (2018) 157. https://doi.org/10.1186/s40168-018-0547-8.

[55]

P. Praveen, F. Jordan, C. Priami, et al., The role of breast-feeding in infant immune system: a systems perspective on the intestinal microbiome, Microbiome 3 (2015) 41. https://doi.org/10.1186/s40168-015-0104-7.

[56]

M. Fallani, D. Young, J. Scott, et al., Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics, J. Pediatr. Gastroenterol. Nutr. 51(1) (2010) 77-84. https://doi.org/10.1097/MPG.0b013e3181d1b11e.

[57]

Ł. Grześkowiak, M.C. Collado, C. Mangani, et al., Distinct gut microbiota in southeastern African and northern European infants, J. Pediatr. Gastroenterol. Nutr. 54(6) (2012) 812-816. https://doi.org/10.1097/MPG.0b013e318249039c.

[58]

Z.T. Lewis, K. Sidamonidze, V. Tsaturyan, et al., The fecal microbial community of breast-fed infants from Armenia and Georgia, Sci. Rep. 7 (2017) 40932. https://doi.org/10.1038/srep40932.

[59]

H.M. Tun, T. Konya, T.K. Takaro, et al., Exposure to household furry pets influences the gut microbiota of infant at 3-4 months following various birth scenarios, Microbiome 5(1) (2017) 40. https://doi.org/10.1186/s40168-017-0254-x.

[60]

M.J. Bonder, A. Kurilshikov, E.F. Tigchelaar, et al., The effect of host genetics on the gut microbiome, Nat. Genet. 48(11) (2018) 1407-1412. https://doi.org/10.1038/ng.3663.

[61]

W. Turpin, O. Espin-Garcia, W. Xu, et al., Association of host genome with intestinal microbial composition in a large healthy cohort, Nat. Genet. 48(11) (2016) 1413-1417. https://doi.org/10.1038/ng.3693.

Food Science and Human Wellness
Pages 1743-1750
Cite this article:
Gao X, Zhang T, Bai X, et al. SMRT sequencing and ddPCR reveal the complexity of developmental trajectories and temporal dynamics of gut bifidobacterial communities in infants. Food Science and Human Wellness, 2023, 12(5): 1743-1750. https://doi.org/10.1016/j.fshw.2023.02.036

643

Views

13

Downloads

0

Crossref

0

Web of Science

0

Scopus

0

CSCD

Altmetrics

Received: 30 July 2021
Revised: 01 November 2021
Accepted: 17 March 2022
Published: 21 March 2023
© 2023 Beijing Academy of Food Sciences.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return