Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation

Generation of genetic diversity is a prerequisite for bacterial evolution and adaptation. Short-term diversification and selection within populations is, however, largely uncharacterised, as existing studies typically focus on fixed substitutions. Here, we use whole-genome deep-sequencing to capture...

Full description

Saved in:
Bibliographic Details
Main Authors: McElroy, Kerensa E., Hui, Janice G. K., Woo, Jerry K. K., Luk, Alison W. S., Webb, Jeremy S., Kjelleberg, Staffan, Rice, Scott A., Thomas, Torsten
Format: Article
Language:English
Published: 2014
Subjects:
Online Access:https://hdl.handle.net/10356/104008
http://hdl.handle.net/10220/19521
Tags: Add Tag
No Tags, Be the first to tag this record!
Institution: Nanyang Technological University
Language: English
id sg-ntu-dr.10356-104008
record_format dspace
spelling sg-ntu-dr.10356-1040082022-02-16T16:28:42Z Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation McElroy, Kerensa E. Hui, Janice G. K. Woo, Jerry K. K. Luk, Alison W. S. Webb, Jeremy S. Kjelleberg, Staffan Rice, Scott A. Thomas, Torsten DRNTU::Science::Biological sciences::Evolution Generation of genetic diversity is a prerequisite for bacterial evolution and adaptation. Short-term diversification and selection within populations is, however, largely uncharacterised, as existing studies typically focus on fixed substitutions. Here, we use whole-genome deep-sequencing to capture the spectrum of mutations arising during biofilm development for two Pseudomonas aeruginosa strains. This approach identified single nucleotide variants with frequencies from 0.5% to 98.0% and showed that the clinical strain 18A exhibits greater genetic diversification than the type strain PA01, despite its lower per base mutation rate. Mutations were found to be strain specific: the mucoid strain 18A experienced mutations in alginate production genes and a c-di-GMP regulator gene; while PA01 acquired mutations in PilT and PilY1, possibly in response to a rapid expansion of a lytic Pf4 bacteriophage, which may use type IV pili for infection. The Pf4 population diversified with an evolutionary rate of 2.43 × 10−3 substitutions per site per day, which is comparable to single-stranded RNA viruses. Extensive within-strain parallel evolution, often involving identical nucleotides, was also observed indicating that mutation supply is not limiting, which was contrasted by an almost complete lack of noncoding and synonymous mutations. Taken together, these results suggest that the majority of the P. aeruginosa genome is constrained by negative selection, with strong positive selection acting on an accessory subset of genes that facilitate adaptation to the biofilm lifecycle. Long-term bacterial evolution is known to proceed via few, nonsynonymous, positively selected mutations, and here we show that similar dynamics govern short-term, within-population bacterial diversification. Published version 2014-06-03T03:44:03Z 2019-12-06T21:24:27Z 2014-06-03T03:44:03Z 2019-12-06T21:24:27Z 2014 2014 Journal Article McElroy, K. E., Hui, J. G. K., Woo, J. K. K., Luk, A. W. S., Webb, J. S., Kjelleberg, S., et al. (2014). Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation. Proceedings of the National Academy of Sciences, 111(14), E1419-E1427. 1091-6490 https://hdl.handle.net/10356/104008 http://hdl.handle.net/10220/19521 10.1073/pnas.1314340111 24706926 en Proceedings of the national academy of sciences © The Author(s). This paper was published in Proceedings of the National Academy of Sciences and is made available as an electronic reprint (preprint) with permission of the Author(s). The paper can be found at the following official DOI: http://dx.doi.org/10.1073/pnas.1314340111.  One print or electronic copy may be made for personal use only. Systematic or multiple reproduction, distribution to multiple locations via electronic or other means, duplication of any material in this paper for a fee or for commercial purposes, or modification of the content of the paper is prohibited and is subject to penalties under law. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic DRNTU::Science::Biological sciences::Evolution
spellingShingle DRNTU::Science::Biological sciences::Evolution
McElroy, Kerensa E.
Hui, Janice G. K.
Woo, Jerry K. K.
Luk, Alison W. S.
Webb, Jeremy S.
Kjelleberg, Staffan
Rice, Scott A.
Thomas, Torsten
Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation
description Generation of genetic diversity is a prerequisite for bacterial evolution and adaptation. Short-term diversification and selection within populations is, however, largely uncharacterised, as existing studies typically focus on fixed substitutions. Here, we use whole-genome deep-sequencing to capture the spectrum of mutations arising during biofilm development for two Pseudomonas aeruginosa strains. This approach identified single nucleotide variants with frequencies from 0.5% to 98.0% and showed that the clinical strain 18A exhibits greater genetic diversification than the type strain PA01, despite its lower per base mutation rate. Mutations were found to be strain specific: the mucoid strain 18A experienced mutations in alginate production genes and a c-di-GMP regulator gene; while PA01 acquired mutations in PilT and PilY1, possibly in response to a rapid expansion of a lytic Pf4 bacteriophage, which may use type IV pili for infection. The Pf4 population diversified with an evolutionary rate of 2.43 × 10−3 substitutions per site per day, which is comparable to single-stranded RNA viruses. Extensive within-strain parallel evolution, often involving identical nucleotides, was also observed indicating that mutation supply is not limiting, which was contrasted by an almost complete lack of noncoding and synonymous mutations. Taken together, these results suggest that the majority of the P. aeruginosa genome is constrained by negative selection, with strong positive selection acting on an accessory subset of genes that facilitate adaptation to the biofilm lifecycle. Long-term bacterial evolution is known to proceed via few, nonsynonymous, positively selected mutations, and here we show that similar dynamics govern short-term, within-population bacterial diversification.
format Article
author McElroy, Kerensa E.
Hui, Janice G. K.
Woo, Jerry K. K.
Luk, Alison W. S.
Webb, Jeremy S.
Kjelleberg, Staffan
Rice, Scott A.
Thomas, Torsten
author_facet McElroy, Kerensa E.
Hui, Janice G. K.
Woo, Jerry K. K.
Luk, Alison W. S.
Webb, Jeremy S.
Kjelleberg, Staffan
Rice, Scott A.
Thomas, Torsten
author_sort McElroy, Kerensa E.
title Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation
title_short Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation
title_full Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation
title_fullStr Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation
title_full_unstemmed Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation
title_sort strain-specific parallel evolution drives short-term diversification during pseudomonas aeruginosa biofilm formation
publishDate 2014
url https://hdl.handle.net/10356/104008
http://hdl.handle.net/10220/19521
_version_ 1725985780437876736