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Engineering >> 2023, Volume 20, Issue 1 doi: 10.1016/j.eng.2021.11.018

Genomic Mutations within the Host Microbiome: Adaptive Evolution or Purifying Selection

a School of Food Science and Engineering, Hainan University, Haikou 570228, China
b Department of Pediatrics, University of California San Diego, La Jolla, CA, 92093, USA
c Center for Microbiome Innovation, Jacobs School of Engineering, University of California San Diego, La Jolla, CA 92093, USA
d Department of Bioengineering, University of California San Diego, La Jolla, CA, 92093, USA
e Department of Computer Science and Engineering, University of California San Diego, La Jolla, CA, 92093, USA

Received: 2021-08-16 Revised: 2021-10-23 Accepted: 2021-11-15 Available online: 2022-01-21

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Abstract

Next-generation sequencing technology has transformed our ability to assess the taxonomic composition functions of host-associated microbiota and microbiomes. More human microbiome research projects—particularly those that explore genomic mutations within the microbiome—will be launched in the next decade. This review focuses on the coevolution of microbes within a microbiome, which shapes strain-level diversity both within and between host species. We also explore the correlation between microbial genomic mutations and common metabolic diseases, and the adaptive evolution of pathogens and probiotics during invasion and colonization. Finally, we discuss advances in methods and algorithms for annotating and analyzing microbial genomic mutations.

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References

[ 1 ] Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012;489(7415):220–30. link1

[ 2 ] Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH. Human microbiome project consortium structure, function and diversity of the healthy human microbiome. Nature 2012;486(7402):207–14. link1

[ 3 ] Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature 2012;486(7402):222–7. link1

[ 4 ] Garud NR, Pollard KS. Population genetics in the human microbiome. Trends Genet 2020;36(1):53–67. link1

[ 5 ] Scanlan PD. Microbial evolution and ecological opportunity in the gut environment. Proc Biol Sci 2019;286(1915):20191964. link1

[ 6 ] Lieberman TD. Seven billion microcosms: evolution within human microbiomes. mSystems 2018;3(2):3. link1

[ 7 ] Zhao S, Lieberman TD, Poyet M, Kauffman KM, Gibbons SM, Groussin M, et al. Adaptive evolution within gut microbiomes of healthy people. Cell Host Microbe 2019;25(5):656–67. link1

[ 8 ] Schloissnig S, Arumugam M, Sunagawa S, Mitreva M, Tap J, Zhu A, et al. Genomic variation landscape of the human gut microbiome. Nature 2013;493 (7430):45–50. link1

[ 9 ] Zeevi D, Korem T, Godneva A, Bar N, Kurilshikov A, Lotan-Pompan M, et al. Structural variation in the gut microbiome associates with host health. Nature 2019;568(7750):43–8. link1

[10] Garud NR, Good BH, Hallatschek O, Pollard KS, Gordo I. Evolutionary dynamics of bacteria in the gut microbiome within and across hosts. PLoS Biol 2019;17 (1):e3000102. link1

[11] Xu Z, Knight R. Dietary effects on human gut microbiome diversity. Br J Nutr 2015;113(S1):S1–5. link1

[12] Roodgar M, Good BH, Garud NR, Martis S, Avula M, Zhou W, et al. Longitudinal linked read sequencing reveals ecological and evolutionary responses of a human gut microbiome during antibiotic treatment. Genome Res 2021;31 (8):1433–46. link1

[13] Scholtens S, Smidt N, Swertz MA, Bakker SJL, Dotinga A, Vonk JM, et al. Cohort profile: LifeLines, a three-generation cohort study and biobank. Int J Epidemiol 2015;44(4):1172–80. link1

[14] Greenblum S, Carr R, Borenstein E. Extensive strain-level copy-number variation across human gut microbiome species. Cell 2015;160(4):583–94. link1

[15] Chen L, Wang D, Garmaeva S, Kurilshikov A, Vich Vila A, Gacesa R, et al. The long-term genetic stability and individual specificity of the human gut microbiome. Cell 2021;184(9):2302–15. link1

[16] Wexler HM. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 2007;20(4):593–621. link1

[17] Nguyen M, Vedantam G. Mobile genetic elements in the genus Bacteroides, and their mechanism(s) of dissemination. Mob Genet Elements 2011;1(3):187–96. link1

[18] Wozniak RAF, Waldor MK. Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 2010;8(8):552–63. link1

[19] Shoemaker NB, Vlamakis H, Hayes K, Salyers AA. Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl Environ Microbiol 2001;67(2):561–8. link1

[20] Vedantam G, Hecht DW. Antibiotics and anaerobes of gut origin. Curr Opin Microbiol 2003;6(5):457–61. link1

[21] Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 2018;555(7695):210–5. link1

[22] De Filippis F, Pasolli E, Ercolini D. Newly explored faecalibacterium diversity is connected to age, lifestyle, geography, and disease. Curr Biol 2020;30 (24):4932–43. link1

[23] Afshin A, Sur PJ, Fay KA, Cornaby L, Ferrara G, Salama JS, et al. Health effects of dietary risks in 195 countries, 1990–2017: a systematic analysis for the global burden of disease study 2017. Lancet 2019;393(10184):1958–72. link1

[24] Zhang R, Wang Z, Fei Y, Zhou B, Zheng S, Wang L, et al. The difference in nutrient intakes between Chinese and Mediterranean, Japanese and American diets. Nutrients 2015;7(6):4661–88. link1

[25] Ma C, Zhang C, Chen D, Jiang S, Shen S, Huo D, et al. Probiotic consumption influences universal adaptive mutations in indigenous human and mouse gut microbiota. Commun Biol 2021;4(1):1198. link1

[26] Ley RE. Gut microbiota in 2015: Prevotella in the gut: choose carefully. Nat Rev Gastroenterol Hepatol 2016;13(2):69–70. link1

[27] Cani PD. Human gut microbiome: hopes, threats and promises. Gut 2018;67 (9):1716–25. link1

[28] Tett A, Huang KD, Asnicar F, Fehlner-Peach H, Pasolli E, Karcher N, et al. The Prevotella copri complex comprises four distinct clades underrepresented in westernized populations. Cell Host Microbe 2019;26(5):666–79. link1

[29] De Filippis F, Pasolli E, Tett A, Tarallo S, Naccarati A, De Angelis M, et al. Distinct genetic and functional traits of human intestinal Prevotella copri strains are associated with different habitual diets. Cell Host Microbe 2019;25 (3):444–53. link1

[30] Sturm R, Haag F, Janicova A, Xu B, Vollrath JT, Bundkirchen K, et al. Acute alcohol consumption increases systemic endotoxin bioactivity for days in healthy volunteers-with reduced intestinal barrier loss in female. Eur J Trauma Emerg Surg. 2022;48(3):1569–77. link1

[31] Zhu Q, Hou Q, Huang S, Ou Q, Huo D, Vázquez-Baeza Y, et al. Compositional and genetic alterations in Graves’ disease gut microbiome reveal specific diagnostic biomarkers. ISME J 2021;15(11):3399–411. link1

[32] McCarroll SA, Altshuler DM. Copy-number variation and association studies of human disease. Nat Genet 2007;39(S7):S37–42. link1

[33] Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, et al. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 2010;329(5991):533–8. link1

[34] Chen Y, Li Z, Hu S, Zhang J, Wu J, Shao N, et al. Gut metagenomes of type 2 diabetic patients have characteristic single-nucleotide polymorphism distribution in Bacteroides coprocola. Microbiome 2017;5(1):15–22. link1

[35] Frazão N, Sousa A, Lässig M, Gordo I. Horizontal gene transfer overrides mutation in Escherichia coli colonizing the mammalian gut. Proc Natl Acad Sci USA 2019;116(36):17906–15. link1

[36] Lescat M, Launay A, Ghalayini M, Magnan M, Glodt J, Pintard C, et al. Using long-term experimental evolution to uncover the patterns and determinants of molecular evolution of an Escherichia coli natural isolate in the streptomycin-treated mouse gut. Mol Ecol 2017;26(7):1802–17. link1

[37] Zhou W, Spoto M, Hardy R, Guan C, Fleming E, Larson PJ, et al. Host-specific evolutionary and transmission dynamics shape the functional diversification of Staphylococcus epidermidis in human skin. Cell 2020;180(3):454–70. link1

[38] Pitout JDD, Nordmann P, Poirel L. Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrob Agents Chemother 2015;59(10):5873–84. link1

[39] Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos GL, Cormican M, et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis 2013;13(9):785–96. link1

[40] Ernst CM, Braxton JR, Rodriguez-Osorio CA, Zagieboylo AP, Li L, Pironti A, et al. Adaptive evolution of virulence and persistence in carbapenem-resistant Klebsiella pneumoniae. Nat Med 2020;26(5):705–11. link1

[41] World Health Organization. Global tuberculosis report 2015. 20th edition. Report. Geneva: World Health Organization; 2015. link1

[42] Lieberman TD, Wilson D, Misra R, Xiong LL, Moodley P, Cohen T, et al. Genomic diversity in autopsy samples reveals within-host dissemination of HIV-associated Mycobacterium tuberculosis. Nat Med 2016;22 (12):1470–4. link1

[43] Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 2014;11(8):506–14. link1

[44] Hou Q, Zhao F, Liu W, Lv R, Khine WWT, Han J, et al. Probiotic-directed modulation of gut microbiota is basal microbiome dependent. Gut Microbes 2020;12(1):1736974. link1

[45] Pamer EG. Resurrecting the intestinal microbiota to combat antibioticresistant pathogens. Science 2016;352(6285):535–8. link1

[46] Cunningham M, Azcarate-Peril MA, Barnard A, Benoit V, Grimaldi R, Guyonnet D, et al. Shaping the future of probiotics and prebiotics. Trends Microbiol 2021;29(8):667–85. link1

[47] Crook N, Ferreiro A, Gasparrini AJ, Pesesky MW, Gibson MK, Wang B, et al. Adaptive strategies of the candidate probiotic E. coli Nissle in the mammalian gut. Cell Host Microbe 2019;25(4):499–512. link1

[48] Mallon CA, Elsas JDV, Salles JF. Microbial invasions: the process, patterns, and mechanisms. Trends Microbiol 2015;23(11):719–29. link1

[49] Ma C, Wasti S, Huang S, Zhang Z, Mishra R, Jiang S, et al. The gut microbiome stability is altered by probiotic ingestion and improved by the continuous supplementation of galactooligosaccharide. Gut Microbes 2020;12 (1):1785252. link1

[50] Kujawska M, La Rosa SL, Roger LC, Pope PB, Hoyles L, McCartney AL, et al. Succession of Bifidobacterium longum strains in response to a changing early life nutritional environment reveals dietary substrate adaptations. iScience 2020;23(8):101368. link1

[51] Cohen PA. Probiotic safety—no guarantees. JAMA Intern Med 2018;178 (12):1577–8. link1

[52] Martino ME, Joncour P, Leenay R, Gervais H, Shah M, Hughes S, et al. Bacterial adaptation to the host’s diet is a key evolutionary force shaping DrosophilaLactobacillus symbiosis. Cell Host Microbe 2018;24(1):109–19. link1

[53] Spinler JK, Sontakke A, Hollister EB, Venable SF, Oh PL, Balderas MA, et al. From prediction to function using evolutionary genomics: human-specific ecotypes of Lactobacillus reuteri have diverse probiotic functions. Genome Biol Evol 2014;6(7):1772–89. link1

[54] Huang S, Jiang S, Huo D, Allaband C, Estaki M, Cantu V, et al. Candidate probiotic Lactiplantibacillus plantarum HNU082 rapidly and convergently evolves within human, mice, and zebrafish gut but differentially influences the resident microbiome. Microbiome 2021;9(1):151. link1

[55] Yelin I, Flett KB, Merakou C, Mehrotra P, Stam J, Snesrud E, et al. Genomic and epidemiological evidence of bacterial transmission from probiotic capsule to blood in ICU patients. Nat Med 2019;25(11):1728–32. link1

[56] Song Y, He Q, Zhang J, Qiao J, Xu H, Zhong Z, et al. Genomic variations in probiotic Lactobacillus plantarum P-8 in the human and rat gut. Front Microbiol 2018;9:893. link1

[57] Feliziani S, Marvig RL, Luján AM, Moyano AJ, Di Rienzo JA, Krogh Johansen H, et al. Coexistence and within-host evolution of diversified lineages of hypermutable Pseudomonas aeruginosa in long-term cystic fibrosis infections. PLoS Genet 2014;10(10):e1004651. link1

[58] Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D, Davis MR, et al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 2011;43(12):1275–80. link1

[59] Treangen TJ, Ondov BD, Koren S, Phillippy AM. The harvest suite for rapid coregenome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014;15(11):524. link1

[60] Loman NJ, Misra RV, Dallman TJ, Constantinidou C, Gharbia SE, Wain J, et al. Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol 2012;30(5):434–9. link1

[61] Steen AD, Crits-Christoph A, Carini P, DeAngelis KM, Fierer N, Lloyd KG, et al. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J 2019;13(12):3126–30. link1

[62] Tramontano M, Andrejev S, Pruteanu M, Klünemann M, Kuhn M, Galardini M, et al. Nutritional preferences of human gut bacteria reveal their metabolic idiosyncrasies. Nat Microbiol 2018;3(4):514–22. link1

[63] Luo C, Knight R, Siljander H, Knip M, Xavier RJ, Gevers D. ConStrains identifies microbial strains in metagenomic datasets. Nat Biotechnol 2015;33(10):1045–52. link1

[64] Nayfach S, Rodriguez-Mueller B, Garud N, Pollard KS. An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography. Genome Res 2016;26(11):1612–25. link1

[65] Costea PI, Munch R, Coelho LP, Paoli L, Sunagawa S, Bork P, et al. metaSNV: A tool for metagenomic strain level analysis. PLoS ONE 2017;12(7):e0182392. link1

[66] Quince C, Delmont TO, Raguideau S, Alneberg J, Darling AE, Collins G, et al. DESMAN: a new tool for de novo extraction of strains from metagenomes. Genome Biol 2017;18(1):181. link1

[67] Olm MR, Crits-Christoph A, Bouma-Gregson K, Firek BA, Morowitz MJ, Banfield JF. inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains. Nat Biotechnol 2021;39 (6):727–36. link1

[68] Truong DT, Tett A, Pasolli E, Huttenhower C, Segata N. Microbial strain-level population structure and genetic diversity from metagenomes. Genome Res 2017;27(4):626–38. link1

[69] Lan F, Demaree B, Ahmed N, Abate AR. Single-cell genome sequencing at ultrahigh-throughput with microfluidic droplet barcoding. Nat Biotechnol 2017;35 (7):640–6. link1

[70] Xu T, Gong Y, Su X, Zhu P, Dai J, Xu J, et al. Phenome-genome profiling of single bacterial cell by Raman-activated gravity-driven encapsulation and sequencing. Small 2020;16(30):e2001172. link1

[71] Jing X, Gong Y, Xu T, Meng Y, Han X, Su X, et al. One-cell metabolic phenotyping and sequencing of soil microbiome by Raman-activated gravitydriven encapsulation (RAGE). mSystems 2021;6(3):e0018121. link1

[72] Brito IL, Yilmaz S, Huang K, Xu L, Jupiter SD, Jenkins AP, et al. Mobile genes in the human microbiome are structured from global to individual scales. Nature 2016;535(7612):435–9. link1

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