Virulence (Dec 2021)

Decreased temperature increases the expression of a disordered bacterial late embryogenesis abundant (LEA) protein that enhances natural transformation

  • Terhi Maula,
  • Nelli Vahvelainen,
  • Helena Tossavainen,
  • Tuuli Koivunen,
  • Marja T. Pöllänen,
  • Anders Johansson,
  • Perttu Permi,
  • Riikka Ihalin

DOI
https://doi.org/10.1080/21505594.2021.1918497
Journal volume & issue
Vol. 12, no. 1
pp. 1239 – 1257

Abstract

Read online

Late embryogenesis abundant (LEA) proteins are important players in the management of responses to stressful conditions, such as drought, high salinity, and changes in temperature. Many LEA proteins do not have defined three-dimensional structures, so they are intrinsically disordered proteins (IDPs) and are often highly hydrophilic. Although LEA-like sequences have been identified in bacterial genomes, the functions of bacterial LEA proteins have been studied only recently. Sequence analysis of outer membrane interleukin receptor I (BilRI) from the oral pathogen Aggregatibacter actinomycetemcomitans indicated that it shared sequence similarity with group 3/3b/4 LEA proteins. Comprehensive nuclearcgq magnetic resonance (NMR) studies confirmed its IDP nature, and expression studies in A. actinomycetemcomitans harboring a red fluorescence reporter protein-encoding gene revealed that bilRI promoter expression was increased at decreased temperatures. The amino acid backbone of BilRI did not stimulate either the production of reactive oxygen species from human leukocytes or the production of interleukin-6 from human macrophages. Moreover, BilRI-specific IgG antibodies could not be detected in the sera of A. actinomycetemcomitans culture-positive periodontitis patients. Since the bilRI gene is located near genes involved in natural competence (i.e., genes associated with the uptake of extracellular (eDNA) and its incorporation into the genome), we also investigated the role of BilRI in these events. Compared to wild-type cells, the ΔbilRI mutants showed a lower transformation efficiency, which indicates either a direct or indirect role in natural competence. In conclusion, A. actinomycetemcomitans might express BilRI, especially outside the host, to survive under stressful conditions and improve its transmission potential.

Keywords