The controversy surrounding the function of DNA uptake

I'm holed up in Indio California, in a "RV Resort" for retirees, working on my grant proposal and checking out the local attractions (Washingtonia palms! The Salton Sea!).

Here's a few paragraphs from the proposal introduction, explaining the big question:

The consequences of DNA uptake are not in question. A cell that takes up DNA inevitably incurs the physiological costs of becoming competent and of transporting the DNA across its envelope. The cell also inevitably gets the incoming DNA’s nucleotides, reducing the demands on its biosynthetic or salvage pathways. Because DNA is abundant in natural environments, and nucleotides are very expensive to synthesize, the nucleotide benefit may be sufficient to compensate for the costs and thus to explain the evolution (origin and continuation) of competence. However if the incoming DNA recombines with the chromosome it may also change the cell’s genotype, which may increase or decrease the cell’s ability to survive and reproduce. The controversial question is whether natural selection on the machinery and regulation of DNA uptake has been influenced by these genetic consequences.

The conventional view is that bacteria take up DNA for recombination (i.e., that recombination has net benefits, and that these are sufficient to account for the evolution of competence). This derives partly from the now-discredited idea that sex in eukaryotes is easily explained by long-term benefits to the species, and partly from observation of ancient beneficial recombination events in bacterial genomes and recent ones in the laboratory. But there are also substantial costs to genetic recombination, because the homologous DNA in the environment comes from dead cells and is likely to carry excess deleterious mutations, and because recombination with heterologous DNA will usually the cell’s well-adapted genetic machinery. These genetic costs are easily overlooked because natural selection eliminates the cells incurring them.

Understanding the evolution of bacterial competence has major implications for our present far-from-satisfactory understanding of why sexual reproduction evolved in eukaryotes. The problematic hypothesis that meiotic sex evolved to create new combinations of genes is often supported by claims that bacterial ‘parasexual’ processes also evolved for this. Because conjugation and transduction are now known to be side effects of selection for more immediate benefits to cells or their genetic parasites, understanding competence is key. If the genetic consequences of competence have not shaped its mechanism or regulation, we will conclude that bacteria get all the genetic variation they need by accident, and thus that meiotic sex is a eukaryotic solution to a eukaryotic problem.

Direct experimental testing of proposed costs and benefits is not the best approach, because it is all too easy to create selection in bacterial cultures, and because laboratory conditions in no way replicate those of the natural environment. Rather, the best way to understand the evolution of competence is to understand its regulation and mechanism. Regulation is informative for all bacteria, as the genes that regulate competence evolved in the natural environment, and understanding the signals they respond to will give us a window on the consequences of competence that have been most beneficial. Because H. influenzae’s uptake specificity causes it to preferentially take up its own DNA, understanding the uptake mechanism responsible for this bias is a critical test of the importance of recombination.