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Genomic characterization of a diazotrophic microbiota associated with maize aerial root mucilage

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  • Shawn M Higdon
  • Tania Pozzo
  • Nguyet Kong
  • Bihua C Huang
  • Mai Lee Yang
  • Richard Jeannotte
  • C Titus Brown
  • Alan B Bennett
  • Bart C Weimer

Abstract

A geographically isolated maize landrace cultivated on nitrogen-depleted fields without synthetic fertilizer in the Sierra Mixe region of Oaxaca, Mexico utilizes nitrogen derived from the atmosphere and develops an extensive network of mucilage-secreting aerial roots that harbors a diazotrophic (N2-fixing) microbiota. Targeting these diazotrophs, we selected nearly 600 microbes of a collection obtained from mucilage and confirmed their ability to incorporate heavy nitrogen (15N2) metabolites in vitro. Sequencing their genomes and conducting comparative bioinformatic analyses showed that these genomes had substantial phylogenetic diversity. We examined each diazotroph genome for the presence of nif genes essential to nitrogen fixation (nifHDKENB) and carbohydrate utilization genes relevant to the mucilage polysaccharide digestion. These analyses identified diazotrophs that possessed the canonical nif gene operons, as well as many other operon configurations with concomitant fixation and release of >700 different 15N labeled metabolites. We further demonstrated that many diazotrophs possessed alternative nif gene operons and confirmed their genomic potential to derive chemical energy from mucilage polysaccharide to fuel nitrogen fixation. These results confirm that some diazotrophic bacteria associated with Sierra Mixe maize were capable of incorporating atmospheric nitrogen into their small molecule extracellular metabolites through multiple nif gene configurations while others were able to fix nitrogen without the canonical (nifHDKENB) genes.

Suggested Citation

  • Shawn M Higdon & Tania Pozzo & Nguyet Kong & Bihua C Huang & Mai Lee Yang & Richard Jeannotte & C Titus Brown & Alan B Bennett & Bart C Weimer, 2020. "Genomic characterization of a diazotrophic microbiota associated with maize aerial root mucilage," PLOS ONE, Public Library of Science, vol. 15(9), pages 1-26, September.
  • Handle: RePEc:plo:pone00:0239677
    DOI: 10.1371/journal.pone.0239677
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    1. Kerstin Unger & Syed Ali Komail Raza & Teresa Mayer & Michael Reichelt & Johannes Stuttmann & Annika Hielscher & Ute Wittstock & Jonathan Gershenzon & Matthew T. Agler, 2024. "Glucosinolate structural diversity shapes recruitment of a metabolic network of leaf-associated bacteria," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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