Charles Darwin would have been honored, fascinated, delighted, but perplexed by a recent gathering of microbiologists

Bernard Dixon

The portrait of evolution painted by Charles Darwin was incomplete, I heard a radio commentator say recently, because he was unaware of "mobile elements-that is, carriers of heredity moving in the biosphere." This must have puzzled many listeners. What about scurrying ants and shoals of fish, acorns and chestnuts falling from trees, wind-borne seeds, spores, and pollen grains? And microorganisms? Darwin was even a bit of amicrobiologist, observing red tides (caused by an autotrophic ciliate classified later as Mesodinium rubrum) from the Beagle during its voyage of 1831- 1836. In addition, he collected many samples of infusoria and examined dust from Beagle's decks and rigging that probably contained diatoms. As several speakers observed during a recent Society for General Microbiology (SGM) meeting in Edinburgh, Scotland, Charles Darwin was interested in microorganisms for another reason- because their existence might be considered a threat to the idea of evolution by natural selection. Why had such "simple" life forms not evolved further? Only in the third edition of Origin of Species, published in 1861 three years after the first, did he tackle this question, arguing that microbes could persist in their "unimproved" state.

It's tempting to speculate which of several subsequent discoveries would have enthralled Darwin the most when he was writing Origin of Species-certainly those mobile elements, transposons, whose recognition was 80 years into the future, and indeed genes themselves, still 40 years ahead.

I rather suspect that he would have been equally intrigued by viruses, whose discovery was also about 40 years over the horizon. Their role in evolution formed an important strand of the SGM meeting, whose participants heard a strong challenge to the traditional view of viruses as components of the tree of life, which saw them as mere by-products of the evolution of cells. By this account, they play only secondary roles in evolution, chiefly by serving as vehicles for cellular genes and by interfering in cellular competition.

Patrick Forterre from the Institut Pasteur in Paris, France, robustly questioned this interpretation. He argued that it rests on a misconception of the real nature of viruses-one that denies the possible existence of true viral genes "born in the virosphere".

"I believe that viruses, defined as capsidencoding organisms, are and always have been the major source of variations that are the substrates for natural selection. Together with derived mobile elements, they provide the principal driving force in the Darwinian evolution of the entire biosphere, at the level of both variation and selection," Forterre said. "They have co-evolved with their hosts, that is to say with the tree of life, and form a tree of their own in the shadow of the cellular tree."

Forterre argued that different families of viruses and related mobile elements co-evolved in each of the three domains of Archaea, Bacteria, and Eukarya. "Although some very ancient families are present in all domains, viruses are very different from one domain to another. Indeed, the existence of three distinct virus domains is a strong argument against scenarios in which one domain originated from another one or from the two others-for example, fusion scenarios between archaea and bacteria for the origin of eukaryotes, or the rooting of the tree of life in one of the three domains."

Marilyn Roossinck of the Samuel Roberts Noble Foundation in Ardmore, Okla., offered a rather different perspective-on viruses as symbionts. Aside from those that are antagonists or commensals, mutualists have been studied only comparatively recently. Acting as unique sources of new genetic information, they can help them to adapt rapidly to extreme shifts in the environment. "This process has clearly happened throughout the evolution of life, and the footprints of these events can be seen in the evidence of past viral integration into the genomes of their hosts, a process of symbiogenesis," Roossinck said. One example of the benefits of mutualistic viruses was their action in protecting plants in Yellowstone National Park that would otherwise die when threatened by big rises in temperature.

During the SGM conference, I found myself wondering what Darwin himself might have made of the proceedings, had he been able to pop in. He would certainly have been gratified to find that his name was cited so frequently, and delighted to see an entire strand of the program named after him. But among the individual papers, two would have held particular fascination for Darwin the voyager, naturalist, and astute observer, while a third would have appealed to Darwin the biologist.

Alexandre Anesio of Bristol University, United Kingdom, and Scott Rogers of Bowling Green State University, Bowling Green, Ohio, who delivered the first two of these papers, documented the existence and even activities of viruses in some of the most extreme, inhospitable locations on the planet. Anesio has been studying microorganisms, including viruses, that colonize small water-filled depressions on the surface of glaciers. Previous investigators have long debated whether this "microbial debris" is virtually dormant or whether it plays any roles in biogeochemical cycles. Studying glaciers in Greenland and elsewhere, Anesio and his colleagues have found that the associated respiration and photosynthesis rates can be comparable with those found in soil in much warmer, more nutrient-rich regions. They have also described a cycle in which bacteria are infected by phages, undergo lysis, and thereby contribute dissolved organic matter that support further bacterial growth.

"The net primary production by glacial ecosystems is large enough to contribute to the in locus utilisation of organic matter and the export of carbon associated with glacial ablation," Anesio reported. "Viruses most probably play an important role in controlling microbial mortality and hence biogeochemical cycling on glaciers. Such processes are relevant to researchers interested in the possibility of extraterrestrial life and the proliferation of terrestrial life forms-during the period of the so-called Snowball Earth."

Reminding his audience in Edinburgh that ice is an excellent matrix for the preservation of microorganisms and nucleic acids, Scott Rogers reported the isolation of both from glacial ice up to 2 million years old and from more recent Antarctic and Arctic lake ice. His metagenomics studies of viruses have provided clues regarding the cellular organisms that inhabit or visit the lakes. An especially intriguing possibility is that influenza A viruses may overwinter, and perhaps survive for decades, in locations frequented by migratory waterfowl.

Given that Darwin could have had little or no conception of what we now term mobile elements of heredity, he would surely be utterly flummoxed by another finding reported in Edinburgh- that of horizontal gene transfer mediated by bacteria which cannot themselves be cultivated and thus apprehended directly by our senses.

The discovery came from Mengqiu Li and coworkers at the University of Sheffield, United Kingdom. Sampling several boreholes in southern England that were contaminated with toluene to various degrees, they isolated five toluene degraders by inoculating groundwater directly onto plates of selective medium containing toluene as the only carbon source. However, as a comparison of the counts of these isolates with the results of staining indicated that they had failed to grow the vast majority of organisms, they used fluorescent in-situ hybridization and other methods to investigate unculturable toluene degraders and their functional genes. This approach allowed them to identify three groups of unculturable bacteria (Pseudomonas sp., Variovorax sp. and Agrobacterium sp.) that were involved in mediating toluene degradation, and to link them with gene functionality.

Darwin's Tree of Life extends very much further than he could possibly have imagined.