Select and resequence reveals relative fitness of bacteria in symbiotic and free-living environments

Liana Burghardt, Brendan Epstein, Joseph Guhlin, Matt Nelson, Margaret R. Taylor, Nevin D Young, Michael J Sadowsky, Peter L Tiffin

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Assays to accurately estimate relative fitness of bacteria growing in multistrain communities can advance our understanding of how selection shapes diversity within a lineage. Here, we present a variant of the “evolve and resequence” approach both to estimate relative fitness and to identify genetic variants responsible for fitness variation of symbiotic bacteria in free-living and host environments. We demonstrate the utility of this approach by characterizing selection by two plant hosts and in two free-living environments (sterilized soil and liquid media) acting on synthetic communities of the facultatively symbiotic bacterium Ensifer meliloti. We find (i) selection that hosts exert on rhizobial communities depends on competition among strains, (ii) selection is stronger inside hosts than in either free-living environment, and (iii) a positive host-dependent relationship between relative strain fitness in multistrain communities and host benefits provided by strains in single-strain experiments. The greatest changes in allele frequencies in response to plant hosts are in genes associated with motility, regulation of nitrogen fixation, and host/rhizobia signaling. The approach we present provides a powerful complement to experimental evolution and forward genetic screens for characterizing selection in bacterial populations, identifying gene function, and surveying the functional importance of naturally occurring genomic variation.

Original languageEnglish (US)
Pages (from-to)2425-2430
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number10
DOIs
StatePublished - Mar 6 2018

Fingerprint

Bacteria
Melilotus
Nitrogen Fixation
Rhizobium
Molecular Evolution
Gene Frequency
Genes
Soil
Population

Keywords

  • Ensifer meliloti
  • Evolve and resequence
  • Facultative mutualism
  • Medicago
  • Synthetic community

PubMed: MeSH publication types

  • Journal Article
  • Research Support, U.S. Gov't, Non-P.H.S.

Cite this

@article{adb9d99dd4544e83a8c0258c6c7ed561,
title = "Select and resequence reveals relative fitness of bacteria in symbiotic and free-living environments",
abstract = "Assays to accurately estimate relative fitness of bacteria growing in multistrain communities can advance our understanding of how selection shapes diversity within a lineage. Here, we present a variant of the “evolve and resequence” approach both to estimate relative fitness and to identify genetic variants responsible for fitness variation of symbiotic bacteria in free-living and host environments. We demonstrate the utility of this approach by characterizing selection by two plant hosts and in two free-living environments (sterilized soil and liquid media) acting on synthetic communities of the facultatively symbiotic bacterium Ensifer meliloti. We find (i) selection that hosts exert on rhizobial communities depends on competition among strains, (ii) selection is stronger inside hosts than in either free-living environment, and (iii) a positive host-dependent relationship between relative strain fitness in multistrain communities and host benefits provided by strains in single-strain experiments. The greatest changes in allele frequencies in response to plant hosts are in genes associated with motility, regulation of nitrogen fixation, and host/rhizobia signaling. The approach we present provides a powerful complement to experimental evolution and forward genetic screens for characterizing selection in bacterial populations, identifying gene function, and surveying the functional importance of naturally occurring genomic variation.",
keywords = "Ensifer meliloti, Evolve and resequence, Facultative mutualism, Medicago, Synthetic community",
author = "Liana Burghardt and Brendan Epstein and Joseph Guhlin and Matt Nelson and Taylor, {Margaret R.} and Young, {Nevin D} and Sadowsky, {Michael J} and Tiffin, {Peter L}",
year = "2018",
month = "3",
day = "6",
doi = "10.1073/pnas.1714246115",
language = "English (US)",
volume = "115",
pages = "2425--2430",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "10",

}

TY - JOUR

T1 - Select and resequence reveals relative fitness of bacteria in symbiotic and free-living environments

AU - Burghardt, Liana

AU - Epstein, Brendan

AU - Guhlin, Joseph

AU - Nelson, Matt

AU - Taylor, Margaret R.

AU - Young, Nevin D

AU - Sadowsky, Michael J

AU - Tiffin, Peter L

PY - 2018/3/6

Y1 - 2018/3/6

N2 - Assays to accurately estimate relative fitness of bacteria growing in multistrain communities can advance our understanding of how selection shapes diversity within a lineage. Here, we present a variant of the “evolve and resequence” approach both to estimate relative fitness and to identify genetic variants responsible for fitness variation of symbiotic bacteria in free-living and host environments. We demonstrate the utility of this approach by characterizing selection by two plant hosts and in two free-living environments (sterilized soil and liquid media) acting on synthetic communities of the facultatively symbiotic bacterium Ensifer meliloti. We find (i) selection that hosts exert on rhizobial communities depends on competition among strains, (ii) selection is stronger inside hosts than in either free-living environment, and (iii) a positive host-dependent relationship between relative strain fitness in multistrain communities and host benefits provided by strains in single-strain experiments. The greatest changes in allele frequencies in response to plant hosts are in genes associated with motility, regulation of nitrogen fixation, and host/rhizobia signaling. The approach we present provides a powerful complement to experimental evolution and forward genetic screens for characterizing selection in bacterial populations, identifying gene function, and surveying the functional importance of naturally occurring genomic variation.

AB - Assays to accurately estimate relative fitness of bacteria growing in multistrain communities can advance our understanding of how selection shapes diversity within a lineage. Here, we present a variant of the “evolve and resequence” approach both to estimate relative fitness and to identify genetic variants responsible for fitness variation of symbiotic bacteria in free-living and host environments. We demonstrate the utility of this approach by characterizing selection by two plant hosts and in two free-living environments (sterilized soil and liquid media) acting on synthetic communities of the facultatively symbiotic bacterium Ensifer meliloti. We find (i) selection that hosts exert on rhizobial communities depends on competition among strains, (ii) selection is stronger inside hosts than in either free-living environment, and (iii) a positive host-dependent relationship between relative strain fitness in multistrain communities and host benefits provided by strains in single-strain experiments. The greatest changes in allele frequencies in response to plant hosts are in genes associated with motility, regulation of nitrogen fixation, and host/rhizobia signaling. The approach we present provides a powerful complement to experimental evolution and forward genetic screens for characterizing selection in bacterial populations, identifying gene function, and surveying the functional importance of naturally occurring genomic variation.

KW - Ensifer meliloti

KW - Evolve and resequence

KW - Facultative mutualism

KW - Medicago

KW - Synthetic community

UR - http://www.scopus.com/inward/record.url?scp=85042936235&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85042936235&partnerID=8YFLogxK

U2 - 10.1073/pnas.1714246115

DO - 10.1073/pnas.1714246115

M3 - Article

C2 - 29453274

AN - SCOPUS:85042936235

VL - 115

SP - 2425

EP - 2430

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 10

ER -