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The Evolutionary Importance of Horizontal DNA Transfer into Animal Germ Lines

Symbiogenetic events included the origin of the eukaryotic cell. This major step enabled all the following evolution leading up to multicellular organisms, including us.
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In a recent blog, I discussed symbiogenesis, one way that sudden large changes have occurred in evolution. Symbiogenetic events included the origin of the eukaryotic cell. This major step enabled all the following evolution leading up to multicellular organisms, including us.

Let me repeat that last point for emphasis. The formation of the eukaryotic cell - setting the stage for all subsequent eukaryotic evolution - did not happen by gradual change and natural selection. That's one major reason why conventional theory is an inadequate explanation of evolution.

Let's look at another source of rapid major change outside conventional theory: horizontal (or lateral) transfer of DNA between cells of different organisms. Many of the commentators on this blog have accepted that horizontal transfer is ubiquitous and frequent between microorganisms. So here we'll take a look at transfer to multicellular organisms.

We know from real-time observations that bacteria can transfer DNA to multicellular organisms. Such transfer is a normal part of the tumor-forming life cycle of the plant pathogen, Agrobacterium tumefaciens, and other bacteria can carry out similar transfers. Laboratory experiments show that E. coli carrying an antibiotic resistance plasmid can transfer it to Chinese Hamster ovary (CHO) cells. In other words, the same apparatus bacteria use to exchange genome segments with each other also works to transfer DNA to the cells of multicellular eukaryotes.

From the symbiosis literature, we also know about many intimate associations of bacteria with animal genitalia. This means there is no physical barrier to DNA exchange between bacteria and animal germ line genomes. The capacity for such transfer was confirmed when investigators found virtually the whole genome of an endosymbiotic bacterium integrated into the chromosomes of its insect host. Similar cases have been reported since.

Some commentators to this blog may be tempted to label these horizontal interkingdom DNA transfers as "random" events leading to the accumulation of what they consider "junk DNA" in the animal genomes. However, there are cases where we know the adaptive significance of the transferred DNA. Among those examples is the evolution of a particular lifestyle allowing nematode worms to occupy a novel ecological niche.

Nematodes are found in all kinds of environments and live by consuming microorganisms (bacteria, archaea and fungi), as parasites, or by predation strategies on other (sometimes larger) animals. A small number of nematodes earn their livings as plant-parasites thanks to horizontal DNA transfer.

The big challenge in living off of plants is in getting at the nutrients enclosed within rigid cell walls built up of cellulose, hemi-cellulose and other polysaccharides (chains composed of sugars linked together chemically). Animals with inside or outside skeletons can accomplish this mechanically. But that route is not available to the soft-bodied nematodes.

An alternative solution for plant pathogenic nematodes is to digest the rigid cell walls with enzymes. The enzymes that break down polysaccharides are called "glycosyl hydrolases," or GHs. They have this name because they use water to break ("hydrolyze") the chemical bonds between sugars ("glyco" means sweet in Greek). To make it easier to keep them straight, these enzymes are classified as GH1s, GH2s, etc.

How is a potentially plant-pathogenic nematode to acquire the GHs it needs to digest the plant host's cell walls? It could evolve them internally, if suitable precursor sequences are present in its genome. But it could also acquire the corresponding DNA from another organism that has already evolved the capacity to digest plant material. The great digesters on the planet, of course, are the microorganisms that recycle all organic matter in the biosphere.

It appears that plant pathogenic nematodes have used the microbial acquisition route at least twice, independently, in their evolution. Here is what was discovered about one group:

"The most damaging nematodes to agriculture worldwide belong to the suborder Tylenchina in clade IV that comprises root-knot nematodes and cyst nematodes, the two most-studied lineages...analysis of the genome of Meloidogyne incognita, the first genome analysis for a plant-parasitic nematode, revealed that the repertoire of cell wall-degrading enzymes in a single species is diverse and abundant..."

Phylogenetic analysis of cell wall degrading protein sequences showed that the capacity to produce them came from bacteria:

"A cluster of GH28 enzymes from the bacterium Ralstonia solanacearum is positioned in the middle of root-knot nematode GH28 enzymes. Interestingly, R. solanacearum is a plant-pathogenic soil bacterium that shares plant hosts with root-knot nematodes..."

A second independent evolution of plant parasitism gave rise to the distantly related pine wilt parasitic nematode. In this case, the enzymes came from fungi and were completely different:

"B. xylophilus GH45 cellulases have not been found in any other nematode genus and are most similar to those from fungi...In a phylogenetic analysis all 11 GH45 proteins found in the B. xylophilus genome are grouped in a highly supported monophyletic group and embedded within a clade of fungal homologues...The absence of GH5 genes in the B. xylophilus genome and the absence of GH45 proteins in Tylenchida nematodes support these hypotheses and suggest that HGT events have repeatedly played important roles in the evolution of plant parasitism in nematodes..."

In both cases, horizontally acquired sequences encoding GH enzymes were amplified and modified within the nematode genomes after horizontal transfer as further steps in evolution of the plant-parasitic lifestyle.

Nematode genomes reveal further horizontal transfer events that help them fill new ecological niches. One case involves acquiring anti-fungal defense proteins from a beetle, whose dead body serves as the food for the fungi that feed the nematode. But that story involves mobile elements and will have to wait for another blog.

What has become clear from these plant-parasitic nematode examples is that horizontal DNA transfers occur into the animal germ line and play a key role in adaptive evolution.

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