Co-evolutionary Signals Identify Burkholderia pseudomallei Survival Strategies in a Hostile Environment

Claire Chewapreecha, Johan Pensar, Supaksorn Chattagul, Maiju Pesonen, Apiwat Sangphukieo, Phumrapee Boonklang, Chotima Potisap, Sirikamon Koosakulnirand, Edward J. Feil, Susanna Dunachie, Narisara Chantratita, Direk Limmathurotsakul, Sharon J. Peacock, Nick P.J. Day, Julian Parkhill, Nicholas R. Thomson, Rasana W. Sermswan, Jukka Corander

Research output: Contribution to journalArticlepeer-review

Abstract

The soil bacterium Burkholderia pseudomallei is the causative agent of melioidosis and a significant cause of human morbidity and mortality in many tropical and subtropical countries. The species notoriously survives harsh environmental conditions but the genetic architecture for these adaptations remains unclear. Here we employed a powerful combination of genome-wide epistasis and co-selection studies (2,011 genomes), condition-wide transcriptome analyses (82 diverse conditions), and a gene knockout assay to uncover signals of "co-selection"-that is a combination of genetic markers that have been repeatedly selected together through B. pseudomallei evolution. These enabled us to identify 13,061 mutation pairs under co-selection in distinct genes and noncoding RNA. Genes under co-selection displayed marked expression correlation when B. pseudomallei was subjected to physical stress conditions, highlighting the conditions as one of the major evolutionary driving forces for this bacterium. We identified a putative adhesin (BPSL1661) as a hub of co-selection signals, experimentally confirmed a BPSL1661 role under nutrient deprivation, and explored the functional basis of co-selection gene network surrounding BPSL1661 in facilitating the bacterial survival under nutrient depletion. Our findings suggest that nutrient-limited conditions have been the common selection pressure acting on this species, and allelic variation of BPSL1661 may have promoted B. pseudomallei survival during harsh environmental conditions by facilitating bacterial adherence to different surfaces, cells, or living hosts.

Original languageEnglish
JournalMolecular Biology and Evolution
Volume39
Issue number1
Early online date18 Oct 2021
DOIs
Publication statusPublished - 31 Jan 2022

Keywords

  • Burkholderia pseudomallei
  • co-selection study
  • nutrient depletion

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

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