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

Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation
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 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.
0027-8424
E1419-E1427
McElroy, K.E.
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Hui, J.G.K.
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Woo, J.K.K.
a631aaec-4e2a-422f-8ae5-9e9eabff0861
Luk, A.W.S.
85f2a099-1cd5-4c63-b3fc-d1465331dde3
Webb, J.S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Kjelleberg, S.
04464230-455d-42c6-999c-72a12ad9d4d4
Rice, S.A.
7733572d-1916-4cad-b156-2ea9bd45d80d
Thomas, T.
a730aea1-d9bc-4561-bd76-bf43ce200861
McElroy, K.E.
5192fba4-9100-44ac-b95e-1bd2416809fb
Hui, J.G.K.
d49dbc69-1355-417e-8e95-0cd8e9c3e2ce
Woo, J.K.K.
a631aaec-4e2a-422f-8ae5-9e9eabff0861
Luk, A.W.S.
85f2a099-1cd5-4c63-b3fc-d1465331dde3
Webb, J.S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Kjelleberg, S.
04464230-455d-42c6-999c-72a12ad9d4d4
Rice, S.A.
7733572d-1916-4cad-b156-2ea9bd45d80d
Thomas, T.
a730aea1-d9bc-4561-bd76-bf43ce200861

McElroy, K.E., Hui, J.G.K., Woo, J.K.K., Luk, A.W.S., Webb, J.S., Kjelleberg, S., Rice, S.A. and Thomas, T. (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. (doi:10.1073/pnas.1314340111). (PMID:24706926)

Record type: Article

Abstract

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.

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Accepted/In Press date: 4 March 2014
e-pub ahead of print date: 28 March 2014
Published date: 8 April 2014
Organisations: Centre for Biological Sciences

Identifiers

Local EPrints ID: 398164
URI: http://eprints.soton.ac.uk/id/eprint/398164
ISSN: 0027-8424
PURE UUID: d1492b35-04d3-48f5-aba1-17fb61292024
ORCID for J.S. Webb: ORCID iD orcid.org/0000-0003-2068-8589

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Date deposited: 20 Jul 2016 12:26
Last modified: 17 Dec 2019 01:45

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