Evolutionary novelty in gravity sensing through horizontal gene transfer and high-order protein assembly

PLoS Biol. 2018 Apr 24;16(4):e2004920. doi: 10.1371/journal.pbio.2004920. eCollection 2018 Apr.

Abstract

Horizontal gene transfer (HGT) can promote evolutionary adaptation by transforming a species' relationship to the environment. In most well-understood cases of HGT, acquired and donor functions appear to remain closely related. Thus, the degree to which HGT can lead to evolutionary novelties remains unclear. Mucorales fungi sense gravity through the sedimentation of vacuolar protein crystals. Here, we identify the octahedral crystal matrix protein (OCTIN). Phylogenetic analysis strongly supports acquisition of octin by HGT from bacteria. A bacterial OCTIN forms high-order periplasmic oligomers, and inter-molecular disulphide bonds are formed by both fungal and bacterial OCTINs, suggesting that they share elements of a conserved assembly mechanism. However, estimated sedimentation velocities preclude a gravity-sensing function for the bacterial structures. Together, our data suggest that HGT from bacteria into the Mucorales allowed a dramatic increase in assembly scale and emergence of the gravity-sensing function. We conclude that HGT can lead to evolutionary novelties that emerge depending on the physiological and cellular context of protein assembly.

MeSH terms

  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Biological Evolution*
  • Cloning, Molecular
  • Escherichia coli / classification
  • Escherichia coli / genetics*
  • Escherichia coli / metabolism
  • Gene Expression
  • Gene Transfer, Horizontal*
  • Genes, Reporter
  • Genetic Vectors / chemistry
  • Genetic Vectors / metabolism
  • Gravitation*
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • HeLa Cells
  • Humans
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Mucorales / classification
  • Mucorales / genetics*
  • Mucorales / metabolism
  • Periplasm / metabolism
  • Phylogeny
  • Protein Multimerization
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Red Fluorescent Protein
  • Vacuoles / metabolism

Substances

  • Bacterial Proteins
  • Luminescent Proteins
  • Recombinant Proteins
  • Green Fluorescent Proteins

Grants and funding

Temasek Life Sciences Laboratory and Singapore Millennium Foundation. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.