Nonmutational mechanism of inheritance in the Archaeon Sulfolobus solfataricus

Sophie Payne, Samuel McCarthy, Tyler Johnson, Erica North, Paul Blum

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Epigenetic phenomena have not yet been reported in archaea, which are presumed to use a classical genetic process of heritability. Here, analysis of independent lineages of Sulfolobus solfataricus evolved for enhanced fitness implicated a non-Mendelian basis for trait inheritance. The evolved strains, called super acid-resistant Crenarchaeota (SARC), acquired traits of extreme acid resistance and genome stability relative to their wild-type parental lines. Acid resistance was heritable because it was retained regardless of extensive passage without selection. Despite the hereditary pattern, in one strain, it was impossible for these SARC traits to result from mutation because its resequenced genome had no mutation. All strains also had conserved, heritable transcriptomes implicated in acid resistance. In addition, they had improved genome stability with absent or greatly decreased mutation and transposition relative to a passaged control. A mechanism that would confer these traits without DNA sequence alteration could involve posttranslationally modified archaeal chromatin proteins. To test this idea, homologous recombination with isogenic DNA was used to perturb native chromatin structure. Recombination at up-regulated loci from the heritable SARC transcriptome reduced acid resistance and gene expression in the majority of recombinants. In contrast, recombination at a control locus that was not part of the heritable transcriptome changed neither acid resistance nor gene expression. Variation in the amount of phenotypic and expression changes across individuals was consistent with Rad54-dependent chromatin remodeling that dictated crossover location and branch migration. These data support an epigenetic model implicating chromatin structure as a contributor to heritable traits.

Original languageEnglish (US)
Pages (from-to)12271-12276
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number48
DOIs
StatePublished - Nov 27 2018

Fingerprint

Sulfolobus solfataricus
Archaea
Acids
Crenarchaeota
Transcriptome
Chromatin
Genomic Instability
Epigenomics
Mutation
Genetic Recombination
Archaeal Proteins
Genetic Phenomena
Gene Expression
Chromatin Assembly and Disassembly
Internal-External Control
Homologous Recombination
Genome

Keywords

  • ALE
  • Archaea
  • Epigenetics
  • Recombination
  • Sulfolobus

ASJC Scopus subject areas

  • General

Cite this

Nonmutational mechanism of inheritance in the Archaeon Sulfolobus solfataricus. / Payne, Sophie; McCarthy, Samuel; Johnson, Tyler; North, Erica; Blum, Paul.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 48, 27.11.2018, p. 12271-12276.

Research output: Contribution to journalArticle

Payne, Sophie ; McCarthy, Samuel ; Johnson, Tyler ; North, Erica ; Blum, Paul. / Nonmutational mechanism of inheritance in the Archaeon Sulfolobus solfataricus. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 48. pp. 12271-12276.
@article{8a4402558063477f920cc9430daf7f8d,
title = "Nonmutational mechanism of inheritance in the Archaeon Sulfolobus solfataricus",
abstract = "Epigenetic phenomena have not yet been reported in archaea, which are presumed to use a classical genetic process of heritability. Here, analysis of independent lineages of Sulfolobus solfataricus evolved for enhanced fitness implicated a non-Mendelian basis for trait inheritance. The evolved strains, called super acid-resistant Crenarchaeota (SARC), acquired traits of extreme acid resistance and genome stability relative to their wild-type parental lines. Acid resistance was heritable because it was retained regardless of extensive passage without selection. Despite the hereditary pattern, in one strain, it was impossible for these SARC traits to result from mutation because its resequenced genome had no mutation. All strains also had conserved, heritable transcriptomes implicated in acid resistance. In addition, they had improved genome stability with absent or greatly decreased mutation and transposition relative to a passaged control. A mechanism that would confer these traits without DNA sequence alteration could involve posttranslationally modified archaeal chromatin proteins. To test this idea, homologous recombination with isogenic DNA was used to perturb native chromatin structure. Recombination at up-regulated loci from the heritable SARC transcriptome reduced acid resistance and gene expression in the majority of recombinants. In contrast, recombination at a control locus that was not part of the heritable transcriptome changed neither acid resistance nor gene expression. Variation in the amount of phenotypic and expression changes across individuals was consistent with Rad54-dependent chromatin remodeling that dictated crossover location and branch migration. These data support an epigenetic model implicating chromatin structure as a contributor to heritable traits.",
keywords = "ALE, Archaea, Epigenetics, Recombination, Sulfolobus",
author = "Sophie Payne and Samuel McCarthy and Tyler Johnson and Erica North and Paul Blum",
year = "2018",
month = "11",
day = "27",
doi = "10.1073/pnas.1808221115",
language = "English (US)",
volume = "115",
pages = "12271--12276",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "48",

}

TY - JOUR

T1 - Nonmutational mechanism of inheritance in the Archaeon Sulfolobus solfataricus

AU - Payne, Sophie

AU - McCarthy, Samuel

AU - Johnson, Tyler

AU - North, Erica

AU - Blum, Paul

PY - 2018/11/27

Y1 - 2018/11/27

N2 - Epigenetic phenomena have not yet been reported in archaea, which are presumed to use a classical genetic process of heritability. Here, analysis of independent lineages of Sulfolobus solfataricus evolved for enhanced fitness implicated a non-Mendelian basis for trait inheritance. The evolved strains, called super acid-resistant Crenarchaeota (SARC), acquired traits of extreme acid resistance and genome stability relative to their wild-type parental lines. Acid resistance was heritable because it was retained regardless of extensive passage without selection. Despite the hereditary pattern, in one strain, it was impossible for these SARC traits to result from mutation because its resequenced genome had no mutation. All strains also had conserved, heritable transcriptomes implicated in acid resistance. In addition, they had improved genome stability with absent or greatly decreased mutation and transposition relative to a passaged control. A mechanism that would confer these traits without DNA sequence alteration could involve posttranslationally modified archaeal chromatin proteins. To test this idea, homologous recombination with isogenic DNA was used to perturb native chromatin structure. Recombination at up-regulated loci from the heritable SARC transcriptome reduced acid resistance and gene expression in the majority of recombinants. In contrast, recombination at a control locus that was not part of the heritable transcriptome changed neither acid resistance nor gene expression. Variation in the amount of phenotypic and expression changes across individuals was consistent with Rad54-dependent chromatin remodeling that dictated crossover location and branch migration. These data support an epigenetic model implicating chromatin structure as a contributor to heritable traits.

AB - Epigenetic phenomena have not yet been reported in archaea, which are presumed to use a classical genetic process of heritability. Here, analysis of independent lineages of Sulfolobus solfataricus evolved for enhanced fitness implicated a non-Mendelian basis for trait inheritance. The evolved strains, called super acid-resistant Crenarchaeota (SARC), acquired traits of extreme acid resistance and genome stability relative to their wild-type parental lines. Acid resistance was heritable because it was retained regardless of extensive passage without selection. Despite the hereditary pattern, in one strain, it was impossible for these SARC traits to result from mutation because its resequenced genome had no mutation. All strains also had conserved, heritable transcriptomes implicated in acid resistance. In addition, they had improved genome stability with absent or greatly decreased mutation and transposition relative to a passaged control. A mechanism that would confer these traits without DNA sequence alteration could involve posttranslationally modified archaeal chromatin proteins. To test this idea, homologous recombination with isogenic DNA was used to perturb native chromatin structure. Recombination at up-regulated loci from the heritable SARC transcriptome reduced acid resistance and gene expression in the majority of recombinants. In contrast, recombination at a control locus that was not part of the heritable transcriptome changed neither acid resistance nor gene expression. Variation in the amount of phenotypic and expression changes across individuals was consistent with Rad54-dependent chromatin remodeling that dictated crossover location and branch migration. These data support an epigenetic model implicating chromatin structure as a contributor to heritable traits.

KW - ALE

KW - Archaea

KW - Epigenetics

KW - Recombination

KW - Sulfolobus

UR - http://www.scopus.com/inward/record.url?scp=85057252552&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85057252552&partnerID=8YFLogxK

U2 - 10.1073/pnas.1808221115

DO - 10.1073/pnas.1808221115

M3 - Article

C2 - 30425171

AN - SCOPUS:85057252552

VL - 115

SP - 12271

EP - 12276

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 - 48

ER -