Horizontal Gene Transfer as an Indispensable Driver for Evolution of Neocallimastigomycota into a Distinct Gut-Dwelling Fungal Lineage

Authors Organisations
  • Chelsea L. Murphy(Author)
    Oklahoma State University - Stillwater
  • Noha H. Youssef(Author)
    Oklahoma State University - Stillwater
  • Radwa A. Hanafy(Author)
    Oklahoma State University - Stillwater
  • M. B. Couger(Author)
    Oklahoma State University - Stillwater
  • Jason E. Stajich(Author)
    University of California, Riverside
  • Yan Wang(Author)
    University of California, Riverside
  • Kristina Baker(Author)
    Oklahoma State University - Stillwater
  • Sumit S. Dagar(Author)
    Agharkar Research Institute
  • Gareth Griffith(Author)
  • Ibrahim F. Farag(Author)
    Oklahoma State University - Stillwater
  • T. M. Callaghan(Author)
    Bavarian State Research Center for Agriculture
  • Mostafa S Elshahed(Author)
    Oklahoma State University - Stillwater
Type Article
Original languageEnglish
Article numbere00988-19
JournalApplied and Environmental Microbiology
Volume85
Early online date18 Jul 2019
DOI
Publication statusE-pub ahead of print - 18 Jul 2019
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Abstract

Survival and growth of the anaerobic gut fungi (AGF; Neocallimastigomycota) in the herbivorous gut necessitate the possession of multiple abilities absent in other fungal lineages. We hypothesized that horizontal gene transfer (HGT) was instrumental in forging the evolution of AGF into a phylogenetically distinct gut-dwelling fungal lineage. The patterns of HGT were evaluated in the transcriptomes of 27 AGF strains, 22 of which were isolated and sequenced in this study, and 4 AGF genomes broadly covering the breadth of AGF diversity. We identified 277 distinct incidents of HGT in AGF transcriptomes, with subsequent gene duplication resulting in an HGT frequency of 2 to 3.5% in AGF genomes. The majority of HGT events were AGF specific (91.7%) and wide (70.8%), indicating their occurrence at early stages of AGF evolution. The acquired genes allowed AGF to expand their substrate utilization range, provided new venues for electron disposal, augmented their biosynthetic capabilities, and facilitated their adaptation to anaerobiosis. The majority of donors were anaerobic fermentative bacteria prevalent in the herbivorous gut. This study strongly indicates that HGT indispensably forged the evolution of AGF as a distinct fungal phylum and provides a unique example of the role of HGT in shaping the evolution of a high-rank taxonomic eukaryotic lineage