دورية أكاديمية
Adaptation and genomic erosion in fragmented Pseudomonas aeruginosa populations in the sinuses of people with cystic fibrosis.
العنوان: | Adaptation and genomic erosion in fragmented Pseudomonas aeruginosa populations in the sinuses of people with cystic fibrosis. |
---|---|
المؤلفون: | Armbruster CR; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Marshall CW; Department of Biological Sciences, Marquette University, Milwaukee, WI 53233, USA., Garber AI; Biodesign Center for Mechanisms of Evolution and School of Life Sciences, Arizona State University, Tempe, AZ 85281, USA., Melvin JA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Zemke AC; Department of Medicine, Division of Pulmonary and Critical Care Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Moore J; Department of Otolaryngology, University of Pittsburgh Medical Center, Pittsburgh, PA 15219, USA., Zamora PF; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Li K; Center for Medicine and the Microbiome, University of Pittsburgh and University of Pittsburgh Medical Center, Pittsburgh, PA 15219, USA., Fritz IL; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Manko CD; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Weaver ML; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Gaston JR; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Morris A; Center for Medicine and the Microbiome, University of Pittsburgh and University of Pittsburgh Medical Center, Pittsburgh, PA 15219, USA., Methé B; Center for Medicine and the Microbiome, University of Pittsburgh and University of Pittsburgh Medical Center, Pittsburgh, PA 15219, USA., DePas WH; Department of Pediatrics, Children's Hospital of Pittsburgh and University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA., Lee SE; Department of Otolaryngology, University of Pittsburgh Medical Center, Pittsburgh, PA 15219, USA. Electronic address: slee192@bwh.harvard.edu., Cooper VS; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA; Center for Medicine and the Microbiome, University of Pittsburgh and University of Pittsburgh Medical Center, Pittsburgh, PA 15219, USA; Pittsburgh Center for Evolutionary Biology & Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA. Electronic address: vaughn.cooper@pitt.edu., Bomberger JM; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA. Electronic address: jbomb@pitt.edu. |
المصدر: | Cell reports [Cell Rep] 2021 Oct 19; Vol. 37 (3), pp. 109829. |
نوع المنشور: | Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't |
اللغة: | English |
بيانات الدورية: | Publisher: Cell Press Country of Publication: United States NLM ID: 101573691 Publication Model: Print Cited Medium: Internet ISSN: 2211-1247 (Electronic) NLM ISO Abbreviation: Cell Rep Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: [Cambridge, MA] : Cell Press, c 2012- |
مواضيع طبية MeSH: | Evolution, Molecular* , Genome, Bacterial* , Mutation*, Cystic Fibrosis/*microbiology , Paranasal Sinuses/*microbiology , Pseudomonas Infections/*microbiology , Pseudomonas aeruginosa/*genetics, Adult ; Cell Line ; Cystic Fibrosis/diagnosis ; Female ; Genetic Drift ; Genotype ; Humans ; Longitudinal Studies ; Male ; Phenotype ; Phylogeny ; Prospective Studies ; Pseudomonas Infections/diagnosis ; Pseudomonas aeruginosa/growth & development |
مستخلص: | Pseudomonas aeruginosa notoriously adapts to the airways of people with cystic fibrosis (CF), yet how infection-site biogeography and associated evolutionary processes vary as lifelong infections progress remains unclear. Here we test the hypothesis that early adaptations promoting aggregation influence evolutionary-genetic trajectories by examining longitudinal P. aeruginosa from the sinuses of six adults with CF. Highly host-adapted lineages harbored mutator genotypes displaying signatures of early genome degradation associated with recent host restriction. Using an advanced imaging technique (MiPACT-HCR [microbial identification after passive clarity technique]), we find population structure tracks with genome degradation, with the most host-adapted, genome-degraded P. aeruginosa (the mutators) residing in small, sparse aggregates. We propose that following initial adaptive evolution in larger populations under strong selection for aggregation, P. aeruginosa persists in small, fragmented populations that experience stronger effects of genetic drift. These conditions enrich for mutators and promote degenerative genome evolution. Our findings underscore the importance of infection-site biogeography to pathogen evolution. Competing Interests: Declaration of interests V.S.C. is a founder of Microbial Genome Sequencing Center, LLC (MiGS) and is a scientific advisor for MiGS. (Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.) |
References: | J Cyst Fibros. 2020 Mar;19 Suppl 1:S47-S53. (PMID: 31685398) Am J Respir Crit Care Med. 2011 Nov 1;184(9):1089-90. (PMID: 22045752) Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2873-8. (PMID: 8610134) Laryngoscope. 2019 Mar;129(3):544-550. (PMID: 30284279) BMC Evol Biol. 2018 Oct 12;18(1):153. (PMID: 30314447) J Bacteriol. 1999 Jan;181(1):107-16. (PMID: 9864319) Paediatr Respir Rev. 2008 Sep;9(3):213-9. (PMID: 18694713) Proc Natl Acad Sci U S A. 2008 Aug 26;105(34):12503-8. (PMID: 18719125) Annu Rev Microbiol. 2020 Sep 8;74:815-834. (PMID: 32692614) Nature. 2016 Aug 11;536(7615):165-70. (PMID: 27479321) Proc Natl Acad Sci U S A. 2006 May 30;103(22):8487-92. (PMID: 16687478) Nat Rev Microbiol. 2011 Nov 08;10(1):13-26. (PMID: 22064560) Crit Rev Microbiol. 2017 Nov;43(6):709-730. (PMID: 28407717) Eur Respir J. 2021 Apr 8;57(4):. (PMID: 33093121) Microbiology (Reading). 2007 May;153(Pt 5):1445-1454. (PMID: 17464058) J Cyst Fibros. 2013 Dec;12(6):729-36. (PMID: 23478131) Sci Transl Med. 2017 Apr 26;9(387):. (PMID: 28446689) Environ Microbiol. 2006 May;8(5):871-84. (PMID: 16623744) Genome Biol Evol. 2021 Aug 3;13(8):. (PMID: 34061185) Front Microbiol. 2020 Jan 31;11:37. (PMID: 32082281) Cell Host Microbe. 2015 Sep 9;18(3):307-19. (PMID: 26299432) Am J Rhinol Allergy. 2013 Sep-Oct;27(5):387-95. (PMID: 24119602) Int Forum Allergy Rhinol. 2018 Mar;8(3):385-388. (PMID: 29210505) J Cyst Fibros. 2018 May;17(3):341-347. (PMID: 29110966) Appl Environ Microbiol. 2009 Dec;75(23):7537-41. (PMID: 19801464) Appl Environ Microbiol. 1990 Jun;56(6):1919-25. (PMID: 2200342) Bioinformatics. 2015 Nov 15;31(22):3691-3. (PMID: 26198102) Genome Biol Evol. 2014 Jan;6(1):76-93. (PMID: 24407854) J Clin Microbiol. 2000 Feb;38(2):818-25. (PMID: 10655391) J Bacteriol. 2001 Feb;183(4):1195-204. (PMID: 11157931) mBio. 2016 Sep 27;7(5):. (PMID: 27677788) J Infect Dis. 2009 Jul 1;200(1):118-30. (PMID: 19459782) Rhinology. 2016 Sep;54(3):206-13. (PMID: 27116399) J Cyst Fibros. 2010 Mar;9(2):130-4. (PMID: 20110197) Nucleic Acids Res. 2021 Jan 8;49(D1):D344-D354. (PMID: 33156333) J Cyst Fibros. 2014 Jul;13(4):449-54. (PMID: 24713592) Cell. 2016 Feb 11;164(4):792-804. (PMID: 26871636) Bioinformatics. 2014 Aug 1;30(15):2114-20. (PMID: 24695404) J Clin Microbiol. 2008 Oct;46(10):3491-3. (PMID: 18685006) Front Cell Infect Microbiol. 2021 Jun 29;11:660007. (PMID: 34268133) Bioinformatics. 2014 May 1;30(9):1312-3. (PMID: 24451623) Proc Natl Acad Sci U S A. 2018 May 1;115(18):4779-4784. (PMID: 29666244) J Bacteriol. 2006 Dec;188(24):8573-85. (PMID: 17041045) mBio. 2010 Sep 21;1(4):. (PMID: 20856824) J Infect Dis. 2007 Jan 1;195(1):70-80. (PMID: 17152010) Antimicrob Agents Chemother. 2020 Apr 21;64(5):. (PMID: 32071060) Nucleic Acids Res. 2005 Jun 02;33(10):3125-32. (PMID: 15933207) Microbiology (Reading). 2002 Jan;148(Pt 1):257-266. (PMID: 11782518) J Bacteriol. 2009 Jun;191(11):3492-503. (PMID: 19329647) Infect Immun. 2003 May;71(5):2775-86. (PMID: 12704152) Appl Environ Microbiol. 1992 Sep;58(9):2886-93. (PMID: 1444402) J Cyst Fibros. 2003 Mar;2(1):29-34. (PMID: 15463843) Mol Microbiol. 2003 Jan;47(1):145-58. (PMID: 12492860) J Bacteriol. 2001 May;183(9):2834-41. (PMID: 11292803) Nat Rev Microbiol. 2012 Dec;10(12):841-51. (PMID: 23147702) PLoS Comput Biol. 2017 Jun 8;13(6):e1005595. (PMID: 28594827) Arch Microbiol. 2006 May;185(4):245-54. (PMID: 16474952) Cytometry. 1993;14(2):136-43. (PMID: 7679962) Am J Respir Crit Care Med. 2014 Jun 1;189(11):1309-15. (PMID: 24702670) J Bacteriol. 1990 Feb;172(2):884-900. (PMID: 2153661) Mol Cell Pediatr. 2017 Dec;4(1):1. (PMID: 28097632) ISME J. 2012 Jan;6(1):31-45. (PMID: 21716309) mBio. 2015 Sep 01;6(5):e00981-15. (PMID: 26330513) Int Forum Allergy Rhinol. 2019 Jul;9(7):759-765. (PMID: 31162888) PLoS Genet. 2014 Oct 16;10(10):e1004651. (PMID: 25330091) FEMS Immunol Med Microbiol. 2012 Jul;65(2):236-44. (PMID: 22211589) Mol Biol Evol. 2022 Jul 2;39(7):. (PMID: 35801562) PLoS Pathog. 2018 Jan 18;14(1):e1006798. (PMID: 29346420) N Engl J Med. 1996 Jul 18;335(3):179-88. (PMID: 8657217) Thorax. 1997 Apr;52(4):318-21. (PMID: 9196512) Curr Opin Microbiol. 2001 Oct;4(5):582-5. (PMID: 11587936) Genome Biol Evol. 2011;3:195-208. (PMID: 21266540) Trends Microbiol. 2016 May;24(5):327-337. (PMID: 26946977) Clin Microbiol Infect. 2010 Jul;16(7):798-808. (PMID: 20880409) J Cyst Fibros. 2012 Dec;11(6):525-31. (PMID: 22595452) J Biol Chem. 1956 Jan;218(1):97-106. (PMID: 13278318) Curr Biol. 2019 Jun 3;29(11):R485-R495. (PMID: 31163163) Int J Med Microbiol. 2010 Dec;300(8):563-72. (PMID: 20837399) J Cyst Fibros. 2018 Mar;17(2):204-212. (PMID: 28826586) Laryngoscope. 1996 Aug;106(8):1005-9. (PMID: 8699890) PLoS Genet. 2013;9(9):e1003741. (PMID: 24039595) BMC Genomics. 2022 Mar 12;23(1):202. (PMID: 35279076) Mol Microbiol. 2007 Apr;64(2):512-33. (PMID: 17493132) Microbiome. 2017 May 12;5(1):53. (PMID: 28494786) Proc Natl Acad Sci U S A. 2016 Feb 9;113(6):1642-7. (PMID: 26729873) J Cyst Fibros. 2015 May;14(3):341-6. (PMID: 25443472) Evolution. 2014 Sep;68(9):2559-70. (PMID: 24910088) Mol Microbiol. 2006 Dec;62(5):1264-77. (PMID: 17059568) J Comput Biol. 2012 May;19(5):455-77. (PMID: 22506599) Biol Direct. 2009 Apr 10;4:13. (PMID: 19361336) Antimicrob Agents Chemother. 2007 Oct;51(10):3776-7. (PMID: 17682099) Curr Opin Microbiol. 2018 Feb;41:8-14. (PMID: 29156371) Bioinformatics. 2013 Apr 15;29(8):1072-5. (PMID: 23422339) Science. 2000 May 19;288(5469):1251-4. (PMID: 10818002) PLoS Genet. 2010 Aug 05;6(8):. (PMID: 20700439) Nat Commun. 2019 Feb 7;10(1):629. (PMID: 30733448) mBio. 2017 Feb 7;8(1):. (PMID: 28174306) Heredity (Edinb). 2014 Nov;113(5):375-80. (PMID: 24849169) FEMS Microbiol Lett. 2004 Jul 1;236(1):137-43. (PMID: 15212803) PLoS Genet. 2020 Jun 12;16(6):e1008848. (PMID: 32530919) Mol Microbiol. 2007 Dec;66(6):1459-73. (PMID: 18028314) Environ Microbiol. 2011 Jul;13(7):1690-704. (PMID: 21492363) Nucleic Acids Res. 2016 Jan 4;44(D1):D646-53. (PMID: 26578582) Antimicrob Agents Chemother. 2005 Jun;49(6):2276-82. (PMID: 15917521) J Bacteriol. 2000 Nov;182(21):5990-6. (PMID: 11029417) J Gen Microbiol. 1955 Dec;13(3):572-81. (PMID: 13278508) Curr Opin Genet Dev. 2004 Dec;14(6):627-33. (PMID: 15531157) Microb Genom. 2020 Sep;6(9):. (PMID: 30946644) Nat Genet. 2003 Sep;35(1):32-40. (PMID: 12910271) Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3807-12. (PMID: 10097119) J Bacteriol. 2012 Dec;194(23):6387-9. (PMID: 22984262) J Cyst Fibros. 2011 Sep;10(5):357-65. (PMID: 21664196) Thorax. 2009 Jun;64(6):535-40. (PMID: 19282318) Nucleic Acids Res. 2016 Jan 4;44(D1):D733-45. (PMID: 26553804) Infect Genet Evol. 2009 Jul;9(4):514-7. (PMID: 19460317) Cell. 2014 Aug 14;158(4):945-958. (PMID: 25088144) Curr Biol. 2017 Nov 20;27(22):3568-3575.e3. (PMID: 29129532) PeerJ. 2015 Oct 08;3:e1319. (PMID: 26500826) Bioinformatics. 2014 Jul 15;30(14):2068-9. (PMID: 24642063) J Cyst Fibros. 2020 Sep;19(5):688-695. (PMID: 32527602) J Cyst Fibros. 2013 Sep;12 Suppl 2:S1-20. (PMID: 24064077) Trends Microbiol. 2013 Sep;21(9):466-74. (PMID: 23827084) Bioinformatics. 2011 Apr 1;27(7):1009-10. (PMID: 21278367) Methods Mol Biol. 2014;1151:165-88. (PMID: 24838886) Front Microbiol. 2015 Sep 29;6:1036. (PMID: 26483767) |
معلومات مُعتمدة: | R61 HL137077 United States HL NHLBI NIH HHS; U01 AI124302 United States AI NIAID NIH HHS; R01 HL123771 United States HL NHLBI NIH HHS; P30 DK072506 United States DK NIDDK NIH HHS; R01 HL142587 United States HL NHLBI NIH HHS; R21 HL143091 United States HL NHLBI NIH HHS; L40 HL104736 United States HL NHLBI NIH HHS; T32 HL129949 United States HL NHLBI NIH HHS; R33 HL137077 United States HL NHLBI NIH HHS; T32 AI049820 United States AI NIAID NIH HHS; R01 HL138630 United States HL NHLBI NIH HHS; T32 AI060525 United States AI NIAID NIH HHS; UL1 TR000005 United States TR NCATS NIH HHS; T35 DK065521 United States DK NIDDK NIH HHS; R00 HL098342 United States HL NHLBI NIH HHS; K23 HL131930 United States HL NHLBI NIH HHS |
فهرسة مساهمة: | Keywords: Pseudomonas aeruginosa; biofilm; chronic rhinosinusitis; cystic fibrosis; genome degradation; host restriction; hybrid assembly; pathoadaptation; pseudogene; sinus |
تواريخ الأحداث: | Date Created: 20211023 Date Completed: 20220215 Latest Revision: 20240404 |
رمز التحديث: | 20240404 |
مُعرف محوري في PubMed: | PMC8667756 |
DOI: | 10.1016/j.celrep.2021.109829 |
PMID: | 34686349 |
قاعدة البيانات: | MEDLINE |
تدمد: | 2211-1247 |
---|---|
DOI: | 10.1016/j.celrep.2021.109829 |