Phage selection for bacterial cheats leads to population decline

While predators and parasites are known for their effects on bacterial population biology, their impact on the dynamics of bacterial social evolution remains largely unclear. Siderophores are iron-chelating molecules that are key to the survival of certain bacterial species in iron-limited environme...

Full description

Saved in:
Bibliographic Details
Published in:Proceedings of the Royal Society B : Biological Sciences Vol. 282; no. 1818; p. 20152207
Main Authors: Vasse, Marie, Torres-Barceló, Clara, Hochberg, Michael E
Format: Journal Article
Language:English
Published: England 07.11.2015
Subjects:
Bacteriophages - physiology
Biological Evolution
Iron - metabolism
Oligopeptides - biosynthesis
Podoviridae - physiology
Pseudomonas aeruginosa - genetics
Pseudomonas aeruginosa - growth & development
Pseudomonas aeruginosa - virology
Selection, Genetic
Siderophores - biosynthesis
Pseudomonas aeruginosa
collective behaviour
experimental evolution
bacteriophage
siderophores
cooperation
ISSN:1471-2954, 1471-2954
Online Access:Get more information
Tags: Add Tag
No Tags, Be the first to tag this record!
Abstract While predators and parasites are known for their effects on bacterial population biology, their impact on the dynamics of bacterial social evolution remains largely unclear. Siderophores are iron-chelating molecules that are key to the survival of certain bacterial species in iron-limited environments, but their production can be subject to cheating by non-producing genotypes. In a selection experiment conducted over approximately 20 bacterial generations and involving 140 populations of the pathogenic bacterium Pseudomonas aeruginosa PAO1, we assessed the impact of a lytic phage on competition between siderophore producers and non-producers. We show that the presence of lytic phages favours the non-producing genotype in competition, regardless of whether iron use relies on siderophores. Interestingly, phage pressure resulted in higher siderophore production, which constitutes a cost to the producers and may explain why they were outcompeted by non-producers. By the end of the experiment, however, cheating load reduced the fitness of mixed populations relative to producer monocultures, and only monocultures of producers managed to grow in the presence of phage in situations where siderophores were necessary to access iron. These results suggest that public goods production may be modulated in the presence of natural enemies with consequences for the evolution of social strategies.
AbstractList While predators and parasites are known for their effects on bacterial population biology, their impact on the dynamics of bacterial social evolution remains largely unclear. Siderophores are iron-chelating molecules that are key to the survival of certain bacterial species in iron-limited environments, but their production can be subject to cheating by non-producing genotypes. In a selection experiment conducted over approximately 20 bacterial generations and involving 140 populations of the pathogenic bacterium Pseudomonas aeruginosa PAO1, we assessed the impact of a lytic phage on competition between siderophore producers and non-producers. We show that the presence of lytic phages favours the non-producing genotype in competition, regardless of whether iron use relies on siderophores. Interestingly, phage pressure resulted in higher siderophore production, which constitutes a cost to the producers and may explain why they were outcompeted by non-producers. By the end of the experiment, however, cheating load reduced the fitness of mixed populations relative to producer monocultures, and only monocultures of producers managed to grow in the presence of phage in situations where siderophores were necessary to access iron. These results suggest that public goods production may be modulated in the presence of natural enemies with consequences for the evolution of social strategies.
While predators and parasites are known for their effects on bacterial population biology, their impact on the dynamics of bacterial social evolution remains largely unclear. Siderophores are iron-chelating molecules that are key to the survival of certain bacterial species in iron-limited environments, but their production can be subject to cheating by non-producing genotypes. In a selection experiment conducted over approximately 20 bacterial generations and involving 140 populations of the pathogenic bacterium Pseudomonas aeruginosa PAO1, we assessed the impact of a lytic phage on competition between siderophore producers and non-producers. We show that the presence of lytic phages favours the non-producing genotype in competition, regardless of whether iron use relies on siderophores. Interestingly, phage pressure resulted in higher siderophore production, which constitutes a cost to the producers and may explain why they were outcompeted by non-producers. By the end of the experiment, however, cheating load reduced the fitness of mixed populations relative to producer monocultures, and only monocultures of producers managed to grow in the presence of phage in situations where siderophores were necessary to access iron. These results suggest that public goods production may be modulated in the presence of natural enemies with consequences for the evolution of social strategies.While predators and parasites are known for their effects on bacterial population biology, their impact on the dynamics of bacterial social evolution remains largely unclear. Siderophores are iron-chelating molecules that are key to the survival of certain bacterial species in iron-limited environments, but their production can be subject to cheating by non-producing genotypes. In a selection experiment conducted over approximately 20 bacterial generations and involving 140 populations of the pathogenic bacterium Pseudomonas aeruginosa PAO1, we assessed the impact of a lytic phage on competition between siderophore producers and non-producers. We show that the presence of lytic phages favours the non-producing genotype in competition, regardless of whether iron use relies on siderophores. Interestingly, phage pressure resulted in higher siderophore production, which constitutes a cost to the producers and may explain why they were outcompeted by non-producers. By the end of the experiment, however, cheating load reduced the fitness of mixed populations relative to producer monocultures, and only monocultures of producers managed to grow in the presence of phage in situations where siderophores were necessary to access iron. These results suggest that public goods production may be modulated in the presence of natural enemies with consequences for the evolution of social strategies.
Author Hochberg, Michael E
Torres-Barceló, Clara
Vasse, Marie
Author_xml – sequence: 1
  givenname: Marie
  surname: Vasse
  fullname: Vasse, Marie
  organization: Institut des Sciences de l'Evolution, CNRS-Université de Montpellier, Place Eugène Bataillon, Montpellier Cedex 5 34095, France
– sequence: 2
  givenname: Clara
  surname: Torres-Barceló
  fullname: Torres-Barceló, Clara
  organization: Institut des Sciences de l'Evolution, CNRS-Université de Montpellier, Place Eugène Bataillon, Montpellier Cedex 5 34095, France
– sequence: 3
  givenname: Michael E
  surname: Hochberg
  fullname: Hochberg, Michael E
  email: mhochber@univ-montp2.fr
  organization: Institut des Sciences de l'Evolution, CNRS-Université de Montpellier, Place Eugène Bataillon, Montpellier Cedex 5 34095, France Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA mhochber@univ-montp2.fr
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26538598$$D View this record in MEDLINE/PubMed
BookMark eNpNjzlPAzEYRC0URA5oKZFLmg0-4qsDReGQIkEB9crHZ7LIWS_r3YJ_TwRBopopnt5o5mjS5hYQuqRkSYnRN33p3JIRKpaMEXWCZnSlaMWMWE3-9Smal_JBCDFCizM0ZVJwLYyeoduXnX0HXCCBH5rc4ph77KwfoG9swn4Hdig4gQ0FDxl3uRuT_QED-NS0cI5Oo00FLo65QG_3m9f1Y7V9fnha320rL4QcKk9kCKvo7WGWc0Mji06I6IE7ygJTjkQTrQZJuQSnlCWBcakFiTwy4zxboOtfb9fnzxHKUO-b4iEl20IeS00Vp0obLuUBvTqio9tDqLu-2dv-q_57zb4BMPtblw
ContentType Journal Article
Copyright 2015 The Author(s).
Copyright_xml – notice: 2015 The Author(s).
DBID CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1098/rspb.2015.2207
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE
MEDLINE - Academic
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Sciences (General)
Biology
EISSN 1471-2954
ExternalDocumentID 26538598
Genre Research Support, Non-U.S. Gov't
Journal Article
GroupedDBID ---
-~X
0R~
29P
2WC
36Y
4.4
5RE
85S
AACGO
AANCE
ABBHK
ABPLY
ABTLG
ABXSQ
ACHIC
ACIWK
ACNCT
ACPRK
ACQIA
ADBBV
ADIYS
ADQXQ
ADULT
AEUPB
AEXZC
AFRAH
ALMA_UNASSIGNED_HOLDINGS
ALMYZ
AOIJS
AQVQM
BAWUL
BTFSW
CGR
CS3
CUY
CVF
DCCCD
DIK
E3Z
EBS
ECM
EIF
EJD
F5P
FRP
GX1
H13
HYE
HZ~
IPSME
JAAYA
JBMMH
JENOY
JHFFW
JKQEH
JLS
JLXEF
JPM
JSG
JST
K-O
KQ8
MRS
NPM
O9-
OK1
RPM
SA0
TR2
W8F
~02
5VS
7X8
ICLEN
RRY
V1E
ID FETCH-LOGICAL-c556t-c06dd4fca8593391f2fb55fce3b12d27b0f9fa8e6136eb77a0d236850f3f29bc2
IEDL.DBID 7X8
ISICitedReferencesCount 18
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000364850200021&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1471-2954
IngestDate Sun Nov 09 11:48:44 EST 2025
Thu Apr 03 07:07:44 EDT 2025
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 1818
Keywords Pseudomonas aeruginosa
collective behaviour
experimental evolution
bacteriophage
siderophores
cooperation
Language English
License 2015 The Author(s).
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c556t-c06dd4fca8593391f2fb55fce3b12d27b0f9fa8e6136eb77a0d236850f3f29bc2
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
OpenAccessLink https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2015.2207
PMID 26538598
PQID 1731789366
PQPubID 23479
ParticipantIDs proquest_miscellaneous_1731789366
pubmed_primary_26538598
PublicationCentury 2000
PublicationDate 2015-11-07
PublicationDateYYYYMMDD 2015-11-07
PublicationDate_xml – month: 11
  year: 2015
  text: 2015-11-07
  day: 07
PublicationDecade 2010
PublicationPlace England
PublicationPlace_xml – name: England
PublicationTitle Proceedings of the Royal Society B : Biological Sciences
PublicationTitleAlternate Proc Biol Sci
PublicationYear 2015
References 18276890 - Science. 2008 Feb 15;319(5865):952-4
22158817 - Science. 2011 Dec 9;334(6061):1398-401
18180746 - ISME J. 2008 Jan;2(1):49-55
23823495 - ISME J. 2013 Nov;7(11):2242-4
16043697 - Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):11076-81
17158317 - Science. 2006 Dec 8;314(5805):1560-3
19070624 - J Theor Biol. 2009 Mar 7;257(1):45-51
13184240 - J Lab Clin Med. 1954 Aug;44(2):301-7
25315099 - Oecologia. 2014 Nov;176(3):607-11
22807479 - Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):12828-33
18704225 - Mol Biosyst. 2008 Sep;4(9):882-8
12410303 - Nature. 2002 Oct 31;419(6910):899-903
25259735 - PLoS One. 2014;9(9):e106628
5875341 - J Theor Biol. 1964 Jul;7(1):1-16
19170825 - J Evol Biol. 2009 Mar;22(3):589-98
22639835 - Ecol Lett. 2012 Aug;15(8):841-6
23418497 - PLoS One. 2013;8(2):e56022
11018148 - Annu Rev Microbiol. 2000;54:881-941
19154373 - Evolution. 2009 Apr;63(4):939-49
20711357 - PLoS Pathog. 2010;6(8):e1000949
16980495 - J Bacteriol. 2006 Oct;188(19):6924-31
22615741 - PLoS One. 2012;7(5):e35833
16777748 - Proc Biol Sci. 2006 Jun 22;273(1593):1529-35
11935015 - Science. 2002 Apr 5;296(5565):72-5
23435883 - Appl Environ Microbiol. 2013 May;79(9):2862-71
12117903 - Infect Immun. 2002 Aug;70(8):3985-93
19232531 - J Microbiol Methods. 2009 May;77(2):207-13
16219778 - Genetics. 2006 Jan;172(1):17-26
23945212 - Biol Lett. 2013 Oct 23;9(5):20130548
25105060 - Bacteriophage. 2014 Jul 08;4:e29866
14977540 - Front Biosci. 2004 May 1;9:1228-339
15329720 - Nature. 2004 Aug 26;430(7003):1024-7
22566647 - Proc Natl Acad Sci U S A. 2012 May 22;109(21):8259-63
23149686 - Mol Syst Biol. 2012;8:621
15184553 - Microbiology. 2004 Jun;150(Pt 6):1671-80
5875340 - J Theor Biol. 1964 Jul;7(1):17-52
20391997 - Ecology. 2010 Feb;91(2):334-40
25024215 - Proc Natl Acad Sci U S A. 2014 Jul 29;111(30):11109-14
19322247 - ISME J. 2009 Jun;3(6):666-74
18059461 - Nature. 2007 Dec 13;450(7172):1079-81
11997446 - Proc Natl Acad Sci U S A. 2002 May 14;99(10):7072-7
22040156 - Environ Microbiol. 2012 Aug;14(8):1830-43
17702577 - Curr Biol. 2007 Aug 21;17(16):1414-9
11796431 - Chest. 2002 Jan;121(1):48-54
22077484 - J Anim Ecol. 2012 Mar;81(2):443-54
8550201 - Infect Immun. 1996 Feb;64(2):518-23
15816912 - Environ Microbiol. 2005 Apr;7(4):459-71
17879185 - Am Nat. 2007 Sep;170(3):331-42
11075711 - Proc Biol Sci. 2000 Oct 7;267(1456):1979-85
24046364 - Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):16056-60
22168669 - J Evol Biol. 2012 Mar;25(3):473-84
5104951 - J Theor Biol. 1971 May;31(2):295-311
23422409 - MBio. 2013;4(1):e00362-12
17206590 - Am Nat. 2007 Jan;169(1):118-29
18479522 - BMC Biol. 2008;6:20
References_xml – reference: 15184553 - Microbiology. 2004 Jun;150(Pt 6):1671-80
– reference: 25315099 - Oecologia. 2014 Nov;176(3):607-11
– reference: 22566647 - Proc Natl Acad Sci U S A. 2012 May 22;109(21):8259-63
– reference: 24046364 - Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):16056-60
– reference: 25105060 - Bacteriophage. 2014 Jul 08;4:e29866
– reference: 17158317 - Science. 2006 Dec 8;314(5805):1560-3
– reference: 20391997 - Ecology. 2010 Feb;91(2):334-40
– reference: 15816912 - Environ Microbiol. 2005 Apr;7(4):459-71
– reference: 11997446 - Proc Natl Acad Sci U S A. 2002 May 14;99(10):7072-7
– reference: 11075711 - Proc Biol Sci. 2000 Oct 7;267(1456):1979-85
– reference: 22615741 - PLoS One. 2012;7(5):e35833
– reference: 16777748 - Proc Biol Sci. 2006 Jun 22;273(1593):1529-35
– reference: 17702577 - Curr Biol. 2007 Aug 21;17(16):1414-9
– reference: 22639835 - Ecol Lett. 2012 Aug;15(8):841-6
– reference: 16219778 - Genetics. 2006 Jan;172(1):17-26
– reference: 11935015 - Science. 2002 Apr 5;296(5565):72-5
– reference: 8550201 - Infect Immun. 1996 Feb;64(2):518-23
– reference: 22040156 - Environ Microbiol. 2012 Aug;14(8):1830-43
– reference: 25024215 - Proc Natl Acad Sci U S A. 2014 Jul 29;111(30):11109-14
– reference: 25259735 - PLoS One. 2014;9(9):e106628
– reference: 15329720 - Nature. 2004 Aug 26;430(7003):1024-7
– reference: 13184240 - J Lab Clin Med. 1954 Aug;44(2):301-7
– reference: 23149686 - Mol Syst Biol. 2012;8:621
– reference: 18059461 - Nature. 2007 Dec 13;450(7172):1079-81
– reference: 5104951 - J Theor Biol. 1971 May;31(2):295-311
– reference: 19232531 - J Microbiol Methods. 2009 May;77(2):207-13
– reference: 18704225 - Mol Biosyst. 2008 Sep;4(9):882-8
– reference: 5875341 - J Theor Biol. 1964 Jul;7(1):1-16
– reference: 18479522 - BMC Biol. 2008;6:20
– reference: 22077484 - J Anim Ecol. 2012 Mar;81(2):443-54
– reference: 16980495 - J Bacteriol. 2006 Oct;188(19):6924-31
– reference: 22168669 - J Evol Biol. 2012 Mar;25(3):473-84
– reference: 22158817 - Science. 2011 Dec 9;334(6061):1398-401
– reference: 19154373 - Evolution. 2009 Apr;63(4):939-49
– reference: 17206590 - Am Nat. 2007 Jan;169(1):118-29
– reference: 12117903 - Infect Immun. 2002 Aug;70(8):3985-93
– reference: 11796431 - Chest. 2002 Jan;121(1):48-54
– reference: 17879185 - Am Nat. 2007 Sep;170(3):331-42
– reference: 19070624 - J Theor Biol. 2009 Mar 7;257(1):45-51
– reference: 11018148 - Annu Rev Microbiol. 2000;54:881-941
– reference: 23418497 - PLoS One. 2013;8(2):e56022
– reference: 23945212 - Biol Lett. 2013 Oct 23;9(5):20130548
– reference: 12410303 - Nature. 2002 Oct 31;419(6910):899-903
– reference: 20711357 - PLoS Pathog. 2010;6(8):e1000949
– reference: 22807479 - Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):12828-33
– reference: 23422409 - MBio. 2013;4(1):e00362-12
– reference: 5875340 - J Theor Biol. 1964 Jul;7(1):17-52
– reference: 23823495 - ISME J. 2013 Nov;7(11):2242-4
– reference: 18180746 - ISME J. 2008 Jan;2(1):49-55
– reference: 23435883 - Appl Environ Microbiol. 2013 May;79(9):2862-71
– reference: 18276890 - Science. 2008 Feb 15;319(5865):952-4
– reference: 19170825 - J Evol Biol. 2009 Mar;22(3):589-98
– reference: 14977540 - Front Biosci. 2004 May 1;9:1228-339
– reference: 16043697 - Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):11076-81
– reference: 19322247 - ISME J. 2009 Jun;3(6):666-74
SSID ssj0009585
Score 2.271102
Snippet While predators and parasites are known for their effects on bacterial population biology, their impact on the dynamics of bacterial social evolution remains...
SourceID proquest
pubmed
SourceType Aggregation Database
Index Database
StartPage 20152207
SubjectTerms Bacteriophages - physiology
Biological Evolution
Iron - metabolism
Oligopeptides - biosynthesis
Podoviridae - physiology
Pseudomonas aeruginosa - genetics
Pseudomonas aeruginosa - growth & development
Pseudomonas aeruginosa - virology
Selection, Genetic
Siderophores - biosynthesis
Title Phage selection for bacterial cheats leads to population decline
URI https://www.ncbi.nlm.nih.gov/pubmed/26538598
https://www.proquest.com/docview/1731789366
Volume 282
WOSCitedRecordID wos000364850200021&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1NS8QwEB3UVfCirp_rFxE86KFukjZJe1IRFy8ue1DYW2nSBAVpV7sK_nsnbXf1IgheemsIk8mbl6_3AE6NYkyFSgVR7i3MYm_zIigNnLCMGZVJRV1tNqGGw3g8TkbthlvVXqucYWIN1Hlp_B55H1tkCourlJeT18C7RvnT1dZCYxE6IVIZn9VqHP8Q3a0tORkCcODPs-aijXEfF43aX-wSF5xT9Tu9rMvMYP2_HdyAtZZgkusmI7qwYItNWGksJz83odtO5oqctYrT51twNXpCWCFV7YmDA0WQyRLd6DhjW8YDdkVeMB0qMi3JZG76RXLrn1babXgc3D7c3AWttUJghJDTwFCZ55EzmZc7CxPmuNNCOGNDzXjOlaYucVlssdhLq5XKaM69VD11oeOJNnwHloqysHtAogwZVoQ0hjsZ6dgkoQmx5mmHK0Gb0KwHJ7N4pZi6_jwiK2z5XqXfEevBbhP0dNJobKRcIhKLJN7_w98HsOpHsn4hqA6h43Di2iNYNh_T5-rtuM4J_A5H91_i8b-x
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Phage+selection+for+bacterial+cheats+leads+to+population+decline&rft.jtitle=Proceedings+of+the+Royal+Society+B+%3A+Biological+Sciences&rft.au=Vasse%2C+Marie&rft.au=Torres-Barcel%C3%B3%2C+Clara&rft.au=Hochberg%2C+Michael+E&rft.date=2015-11-07&rft.issn=1471-2954&rft.eissn=1471-2954&rft.volume=282&rft.issue=1818&rft.spage=20152207&rft_id=info:doi/10.1098%2Frspb.2015.2207&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1471-2954&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1471-2954&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1471-2954&client=summon