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Inheritance outside the family

Exchange of genes among different species is a source of debate among evolutionists

Increasingly more academics are showing that genetic characteristics are not only transmitted from parents to children, as the principles of heredity suppose, but circulate among different species. It is not new that bacteria can acquire genes that make them more infectious or that allow them to survive under adverse conditions. Now the group of molecular biologist, Carlos Menck, from the Institute of Biomedical Sciences at the University of São Paulo (ICB-USP), has shown that part of the metabolism of the Xanthomonas bacteria that cause the citric cancer that attacks orange and lemon trees, is different from most other bacteria. The difference comes from the possibility of the exchange of genes between species, which is known as lateral transfer and which even has some researchers arguing that Charles Darwin was wrong, when 150 years ago he used the branch structure of a tree to describe the evolution of biological diversity.

Menck’s discoveries began with his fortuitous observations while carrying out the first Brazilian genome sequencing projects.  While he was working towards unveiling the genetic material of the Xylella and Xanthomonas bacteria, which are very important because of the diseases they cause in plantations, he noticed that many of the genes seemed not to be transmitted throughout the bacteria strains. That is where Wanessa Lima’s PhD came into the picture. She detected various cases of the lateral transfer of genes in these bacteria, as she reported in 2008 in the Journal of Molecular Evolution and FEMS Microbiology Letters.

There were even accessory genes that did not challenge the premise that functions that are essential to life cannot be copied by other organisms. Now all this has changed: Wanessa discovered that bacteria of the Xanthomonadales and Flavobacteriales orders fabricate a compound that is essential for generating energy (nicotinamide adenine dinucleotide – NAD) using a sequence of biochemical reactions so far known only in eukaryotes, organisms in which the genetic material is packaged within the nucleus. Eukaryotes may be simple, like fungi composed of independent cells, or more complex and multicellular, like people. Bacteria, on the other hand, are prokaryotes: most of the time they are unicellular and lack a nucleus, and generally have a circular DNA molecule.

The result, which was published in February in Molecular Biology and Evolution, is helping us to understand  bacteria because this is the first described case of a vital function, the genes of which have been substituted. “It’s most probable that the genes were exchanged between an ancestral eukaryote and an ancestral bacteria and later spread by speciation in Xanthomonas or flavobacteria”, imagines the researcher. Based on his search for similar genes in an international genetic sequencing bank, Menck is betting on this ancestral eukaryote donor being a fungus that coexisted with the bacteria, a host, in symbiosis or in the ground, probably a little after the separation of Xanthomonas and Xylella, some 15 million years ago. In a way that has yet to be clarified, this proximity allowed strands of DNA to pass from one species to another, with or without the help of a virus.

The group from USP is still unable to explain why in these bacteria the new way of fabricating DNA substituted what already existed. “The eukaryote route is more costly in terms of nutrients and energy, in addition to demanding more oxygen”, says Wanessa. She suspects that this new route was retained by Xanthomonas and flavobacteriales because it had advantages given the amino acids available or the level of oxygen in the environment. As far as Menck is concerned natural selection is probably behind their permanent state. The as-yet-unpublished work of one of his students, Apuã Paquola, who works with bioinformatics, shows that some 20% of bacteria genomes come from lateral transfer among bacteria from different groups. These are the strands that were favored by evolution and became established. The signs are that the exchange of genes between different living beings is constant, but generally new combinations are lost during evolution.

Even so, some researchers argue that the lateral transfer of genes make the tree metaphor for describing the evolution of biodiversity wrong, a controversy that in January was the cover story of the British journal, New Scientist. In the tree, current species are on the tip of each branch and the points where they divide represent common ancestors. But in an article published in Nucleic Acids Research, molecular biologist, Eugene Koonin, from the National Institutes of Health (NIH) in the United States, argues that the genetic heritage of bacteria is entirely interlinked, like a sea of genes without anything separating them. In his opinion this invalidates the tree of life concept: “These findings give body to a new and dynamic vision of the prokaryote world that is better represented as a complex network of genetic elements that exchange genes at very variable rates”, he writes.

The controversy promises to run and run. For John Wilkins, a science philosopher from the University of Queensland, in Australia, the view of evolution as a network is wrong. “If one species was formed by generalized genetic transfer”, he says, “in such a way that it was impossible to say what is inherited and what isn’t I think it would be difficult to call it a species”. But he believes that the probability of this happening is extremely remote. Menck adds: there might be a genetic mixture between species, but the genes themselves follow strains, as set out in Darwin’s theory of evolution. Exchanges make the work of anyone who is looking to reconstruct bacterial genealogy difficult, but the researcher from USP points out that in addition to the fact that 80% of the prokaryote genes are transferred by descendency, some never become ready to be transferred. It is this fixed element of genetic material that allows the family relationships among bacteria to be reconstructed. “The network is more like a fine spider’s web covering the tree and not the opposite”, he concludes.

According to Menck, the controversy is a positive thing and helps researchers understand more and more about evolution processes. From this point of view, the conclusion of Koonin’s article may be encouraging: “The complexity emerging from the prokaryote world is beyond our reach at present. We don’t have the appropriate language in terms of theories and tools to describe the functioning and stories of the genomic network. Developing this language is the biggest challenge for the next step in the genomic evolution of prokaryotes”.

The project
DNA repair genes: Functional analysis and evolution (nº 03/13255-5); Modality: Thematic project; Coordinator: Carlos Frederico Martins Menck – ICB-USP; Investment: R$ 1,453,233.23

Scientific articles
LIMA, W. C. et al. NAD biosynthesis evolution in bacteria: lateral gene transfer of kyurenine pathway in Xanthomonadales and Flavobacteriales. Molecular Biology and Evolution. v. 26, n. 2, p. 399-405. Feb. 2009.
KOONIN, E. V. e WOLF, Y. I. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Research. v. 36, n. 21, p. 6.688-6.719. Dec. 2008.
WILKINS, J. S. The concept and causes of microbial species. History and Philosophy of the Life Sciences. v. 28, n. 3, p. 389-407. 2006.