Biosynthesis of vitamins and cofactors in bacterium-harbouring trypanosomatids depends on the symbiotic association as revealed by genomic analyses

PLoS One. 2013 Nov 19;8(11):e79786. doi: 10.1371/journal.pone.0079786. eCollection 2013.

Abstract

Some non-pathogenic trypanosomatids maintain a mutualistic relationship with a betaproteobacterium of the Alcaligenaceae family. Intensive nutritional exchanges have been reported between the two partners, indicating that these protozoa are excellent biological models to study metabolic co-evolution. We previously sequenced and herein investigate the entire genomes of five trypanosomatids which harbor a symbiotic bacterium (SHTs for Symbiont-Haboring Trypanosomatids) and the respective bacteria (TPEs for Trypanosomatid Proteobacterial Endosymbiont), as well as two trypanosomatids without symbionts (RTs for Regular Trypanosomatids), for the presence of genes of the classical pathways for vitamin biosynthesis. Our data show that genes for the biosynthetic pathways of thiamine, biotin, and nicotinic acid are absent from all trypanosomatid genomes. This is in agreement with the absolute growth requirement for these vitamins in all protozoa of the family. Also absent from the genomes of RTs are the genes for the synthesis of pantothenic acid, folic acid, riboflavin, and vitamin B6. This is also in agreement with the available data showing that RTs are auxotrophic for these essential vitamins. On the other hand, SHTs are autotrophic for such vitamins. Indeed, all the genes of the corresponding biosynthetic pathways were identified, most of them in the symbiont genomes, while a few genes, mostly of eukaryotic origin, were found in the host genomes. The only exceptions to the latter are: the gene coding for the enzyme ketopantoate reductase (EC:1.1.1.169) which is related instead to the Firmicutes bacteria; and two other genes, one involved in the salvage pathway of pantothenic acid and the other in the synthesis of ubiquinone, that are related to Gammaproteobacteria. Their presence in trypanosomatids may result from lateral gene transfer. Taken together, our results reinforce the idea that the low nutritional requirement of SHTs is associated with the presence of the symbiotic bacterium, which contains most genes for vitamin production.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Betaproteobacteria / genetics*
  • Betaproteobacteria / metabolism
  • Biological Factors / biosynthesis*
  • Biological Factors / genetics
  • Biological Factors / metabolism
  • Biosynthetic Pathways / genetics*
  • Genome, Protozoan / genetics
  • Genomics / methods
  • Phylogeny
  • Symbiosis / genetics*
  • Trypanosoma / genetics*
  • Trypanosoma / metabolism
  • Trypanosoma / microbiology*
  • Vitamins / biosynthesis*
  • Vitamins / genetics
  • Vitamins / metabolism

Substances

  • Biological Factors
  • Vitamins

Grant support

The research leading to these results was funded by: the European Research Council under the European Community's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement n°[247073]10; the French project ANR MIRI BLAN08-1335497; FAPERJ grant coordinated by Dr. Cristina Motta and the FAPERJ-INRIA project RAMPA; by the Laboratoire International Associé (LIA) LIRIO co-coordinated by Ana Tereza R. de Vasconcelos (Labinfo, LNCC, Brazil) and Marie-France Sagot (LBBE, UCBL-CNRS-INRIA, France); the National Science Foundation [USA, grant number NSF DEB-0830056 to Gregory Buck]; and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) to Cristina Motta, Marta M. G. Teixeira and Erney P. Camargo. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.