Mutation Accumulation and Horizontal Gene Transfer in Colonizing the Gut of Old Mice

Overview

Journal Commun Integr Biol

Specialty Biology

Date 2020 Oct 5

PMID 33014261

Citations 6

Authors

Hugo C Barreto

Nelson Frazao

Ana Sousa

Anke Konrad

Isabel Gordo

Affiliations

Soon will be listed here.

Abstract

The ecology and environment of the microbes that inhabit the mammalian intestine undergoes several changes as the host ages. Here, we ask if the selection pressure experienced by a new strain colonizing the aging gut differs from that in the gut of young adults. Using experimental evolution in mice after a short antibiotic treatment, as a model for a common clinical situation, we show that a new colonizing strain rapidly adapts to the aging gut via both mutation accumulation and bacteriophage-mediated horizontal gene transfer (HGT). The pattern of evolution of in aging mice is characterized by a larger number of transposable element insertions and intergenic mutations compared to that in young mice, which is consistent with the gut of aging hosts harboring a stressful and iron limiting environment.

Citing Articles

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References

Deatherage D, Traverse C, Wolf L, Barrick J . Detecting rare structural variation in evolving microbial populations from new sequence junctions using breseq. Front Genet. 2015; 5:468. PMC: 4301190. DOI: 10.3389/fgene.2014.00468. View

Robinson J, Thorvaldsdottir H, Wenger A, Zehir A, Mesirov J . Variant Review with the Integrative Genomics Viewer. Cancer Res. 2017; 77(21):e31-e34. PMC: 5678989. DOI: 10.1158/0008-5472.CAN-17-0337. View

Sausset R, Petit M, Gaboriau-Routhiau V, De Paepe M . New insights into intestinal phages. Mucosal Immunol. 2020; 13(2):205-215. PMC: 7039812. DOI: 10.1038/s41385-019-0250-5. View

Chen S, Zhou Y, Chen Y, Gu J . fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018; 34(17):i884-i890. PMC: 6129281. DOI: 10.1093/bioinformatics/bty560. View

Lee W, Stromberg M, Ward A, Stewart C, Garrison E, Marth G . MOSAIK: a hash-based algorithm for accurate next-generation sequencing short-read mapping. PLoS One. 2014; 9(3):e90581. PMC: 3944147. DOI: 10.1371/journal.pone.0090581. View

Nairz M, Weiss G . Iron in infection and immunity. Mol Aspects Med. 2020; 75:100864. DOI: 10.1016/j.mam.2020.100864. View

Wawer A, Jennings A, Fairweather-Tait S . Iron status in the elderly: A review of recent evidence. Mech Ageing Dev. 2018; 175:55-73. DOI: 10.1016/j.mad.2018.07.003. View

Khademi S, Sazinas P, Jelsbak L . Within-Host Adaptation Mediated by Intergenic Evolution in Pseudomonas aeruginosa. Genome Biol Evol. 2019; 11(5):1385-1397. PMC: 6505451. DOI: 10.1093/gbe/evz083. View

Blumer C, Kleefeld A, Lehnen D, Heintz M, Dobrindt U, Nagy G . Regulation of type 1 fimbriae synthesis and biofilm formation by the transcriptional regulator LrhA of Escherichia coli. Microbiology (Reading). 2005; 151(Pt 10):3287-3298. DOI: 10.1099/mic.0.28098-0. View

10.

Treepong P, Guyeux C, Meunier A, Couchoud C, Hocquet D, Valot B . panISa: ab initio detection of insertion sequences in bacterial genomes from short read sequence data. Bioinformatics. 2018; 34(22):3795-3800. DOI: 10.1093/bioinformatics/bty479. View

11.

Hawkey J, Hamidian M, Wick R, Edwards D, Billman-Jacobe H, Hall R . ISMapper: identifying transposase insertion sites in bacterial genomes from short read sequence data. BMC Genomics. 2015; 16:667. PMC: 4558774. DOI: 10.1186/s12864-015-1860-2. View

12.

Ng K, Aranda-Diaz A, Tropini C, Frankel M, Van Treuren W, OLoughlin C . Recovery of the Gut Microbiota after Antibiotics Depends on Host Diet, Community Context, and Environmental Reservoirs. Cell Host Microbe. 2019; 26(5):650-665.e4. PMC: 8276089. DOI: 10.1016/j.chom.2019.10.011. View

13.

Li H, Durbin R . Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010; 26(5):589-95. PMC: 2828108. DOI: 10.1093/bioinformatics/btp698. View

14.

Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao J . Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 2016; 16:90. PMC: 4879732. DOI: 10.1186/s12866-016-0708-5. View

15.

Hamner S, McInnerney K, Williamson K, Franklin M, Ford T . Bile salts affect expression of Escherichia coli O157:H7 genes for virulence and iron acquisition, and promote growth under iron limiting conditions. PLoS One. 2013; 8(9):e74647. PMC: 3769235. DOI: 10.1371/journal.pone.0074647. View

16.

Barroso-Batista J, Sousa A, Lourenco M, Bergman M, Sobral D, Demengeot J . The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps. PLoS Genet. 2014; 10(3):e1004182. PMC: 3945185. DOI: 10.1371/journal.pgen.1004182. View

17.

Preumont A, Snoussi K, Stroobant V, Collet J, Van Schaftingen E . Molecular identification of pseudouridine-metabolizing enzymes. J Biol Chem. 2008; 283(37):25238-25246. DOI: 10.1074/jbc.M804122200. View

18.

Barrick J, Colburn G, Deatherage D, Traverse C, Strand M, Borges J . Identifying structural variation in haploid microbial genomes from short-read resequencing data using breseq. BMC Genomics. 2014; 15:1039. PMC: 4300727. DOI: 10.1186/1471-2164-15-1039. View

19.

Fulop T, Larbi A, Dupuis G, Le Page A, Frost E, Cohen A . Immunosenescence and Inflamm-Aging As Two Sides of the Same Coin: Friends or Foes?. Front Immunol. 2018; 8:1960. PMC: 5767595. DOI: 10.3389/fimmu.2017.01960. View

20.

Maharjan R, Ferenci T . A shifting mutational landscape in 6 nutritional states: Stress-induced mutagenesis as a series of distinct stress input-mutation output relationships. PLoS Biol. 2017; 15(6):e2001477. PMC: 5464527. DOI: 10.1371/journal.pbio.2001477. View