Bioinformatics analysis of bacterial annexins--putative ancestral relatives of eukaryotic annexins

PLoS One. 2014 Jan 16;9(1):e85428. doi: 10.1371/journal.pone.0085428. eCollection 2014.

Abstract

Annexins are Ca(2+)-binding, membrane-interacting proteins, widespread among eukaryotes, consisting usually of four structurally similar repeated domains. It is accepted that vertebrate annexins derive from a double genome duplication event. It has been postulated that a single domain annexin, if found, might represent a molecule related to the hypothetical ancestral annexin. The recent discovery of a single-domain annexin in a bacterium, Cytophaga hutchinsonii, apparently confirmed this hypothesis. Here, we present a more complex picture. Using remote sequence similarity detection tools, a survey of bacterial genomes was performed in search of annexin-like proteins. In total, we identified about thirty annexin homologues, including single-domain and multi-domain annexins, in seventeen bacterial species. The thorough search yielded, besides the known annexin homologue from C. hutchinsonii, homologues from the Bacteroidetes/Chlorobi phylum, from Gemmatimonadetes, from beta- and delta-Proteobacteria, and from Actinobacteria. The sequences of bacterial annexins exhibited remote but statistically significant similarity to sequence profiles built of the eukaryotic ones. Some bacterial annexins are equipped with additional, different domains, for example those characteristic for toxins. The variation in bacterial annexin sequences, much wider than that observed in eukaryotes, and different domain architectures suggest that annexins found in bacteria may actually descend from an ancestral bacterial annexin, from which eukaryotic annexins also originate. The hypothesis of an ancient origin of bacterial annexins has to be reconciled with the fact that remarkably few bacterial strains possess annexin genes compared to the thousands of known bacterial genomes and with the patchy, anomalous phylogenetic distribution of bacterial annexins. Thus, a massive annexin gene loss in several bacterial lineages or very divergent evolution would appear a likely explanation. Alternative evolutionary scenarios, involving horizontal gene transfer between bacteria and protozoan eukaryotes, in either direction, appear much less likely. Altogether, current evidence does not allow unequivocal judgement as to the origin of bacterial annexins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Annexins / chemistry
  • Annexins / genetics*
  • Bacteria / genetics
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics*
  • Computational Biology
  • Conserved Sequence
  • Humans
  • Molecular Sequence Annotation
  • Molecular Sequence Data
  • Phylogeny
  • Protein Structure, Tertiary

Substances

  • Annexins
  • Bacterial Proteins

Grant support

This work was supported by the NODPERCEPTION contract (MRTN-CT-2006-035546) from the European Community's Marie Curie Research Training Network Program and by the Nencki Institute of Experimental Biology, Warsaw, Poland. PKK acknowledges a fellowship from the EC NODPERCEPTION contract No ESR7. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.