From bioremediation to communicable disease control, ecological perspectives are more important than ever for microbiologists

Bernard Dixon

Some of the world's most polluted soil is to be found in abandoned chemical plants and similar facilities in the former Soviet bloc countries of Eastern Europe. Indeed, sites such as derelict gas works now offer enticing challenges to bioremediators. Introduce appropriate cocktails of microbial scavengers, and/or stimulate those already present by aeration or nourishment, and you have an efficient way of eliminating unwanted xenobiotics.

But there is another approach. We might decide to leave contaminated areas entirely alone. We might even protect them-to conserve the unique microbiological resources they may contain. The suggestion comes from Willy Verstraete, head of the Laboratory of Ecology and Technology at Ghent University, Belgium, and he is well aware that it is controversial.

Yet the logic seems impeccable. Just as extreme environments around the world have proved happy hunting grounds for prospectors seeking organisms of use in industry, so the toxic environments spawned by technological activities may have created ideal conditions for other extraordinary microbes to evolve. Little has been done so far to scrutinize polluted sites from this angle. Yet the potential must be there. Willy Verstraete has also bought into the "hygiene hypothesis," now gaining strength, which sees microbiologically cleaner environments as partially responsible for increasing allergies and other problems stemming from understimulation of the immune system.

Both ideas featured in a Society for Applied Microbiology lecture delivered recently in London. In his talk, Verstraete argued for greater focus on microbial ecology and for more calculated management of microbial resources, whether in environmental biotechnology, clinical practice, or other sectors of applied microbiology. He sees this perspective as vital to our handling of the 21st century's "super-challenges," from climate change and renewable energy sources to the threat of new pandemics and the general demise of environmental quality. While the importance of ecological investigation and analysis is well established in Willy's own field, it holds a less central role in the realm of infectious disease. This is ironic, since it is now 50 years since Rene Dubos, in Mirage of Health (Allen & Unwin, 1960), urged the merits of ecological thinking in our approach to infection control. "Complete freedom from disease and from struggle is almost incompatible with the process of living," Dubos wrote. "Mankind's dream of perfect health for all in an antiseptic Eden is not only impossible, but impractical. And the aseptic world would be dangerous as well as woefully dull."

Some critics felt that these remarks were naı ¨ve. Yet a rereading of the book today reveals not only a remarkable anticipation of the hygiene hypothesis but also some far-seeing verities regarding social determinants of health, social patterns of disease, and the importance of the environment in mediating the interplay between human, animal, and plant pathogens and their target species. Dubos did not minimize the significance of specific etiology and its practical application-he was, after all, a pioneer of antibiotics. But he felt keenly that we should reject simplistic concepts of pathogens and their hosts.

"Ancient physicians knew that the severity and prevalence of various diseases differed greatly according to the geographical area, the time, the social customs, and economic status, the occupation," Dubos wrote. At that time, half a century ago, he believed that medical microbiology, despite its unquestioned triumphs, had lost touch with this broader picture. He might well entertain similar thoughts regarding molecular genetics today.

By coincidence, two recent papers have reminded us of the importance of seeing communicable diseases in their ecological context. One comes from the United Kingdom, the other from Spain.

The first describes an attempt to discern the reason(s) why Escherichia coli O157:H7 infections are much commoner in Scotland than in England and Wales. The organism first came to light, of course, in the United States 25 years ago. Following that initial, sporadic case of hemorrhagic colitis, it emerged as the cause of most cases of hemolytic uremic syndrome (HUS). E. coli O157:H7 subsequently hit the headlines as the source of a hemorrhagic colitis outbreak attributed to contaminated beef burgers. Over the past decade, it has caused infections, some with serious consequences, not only in the United States but also in Canada, the United Kingdom, Sweden, and Japan.

Within the United Kingdom, the worst incident on record was an outbreak of food poisoning in Scotland in 1996. There were 16 deaths among 120 patients, 34 of whom developed HUS. E. coli O157:H7 is common in cattle, and although they, as well as sheep and goats, provide natural reservoirs for the organism, they are apparently unaffected by it. Given this widespread distribution-and an infectious dose of fewer than 100 cells- outbreaks are less common than might be expected. The explanation may be that only certain strains infect humans.

Another puzzle is why E. coli O157:H7 causes 3% of all laboratory-confirmed cases of food poisoning in Scotland, as compared with only 1% in England and Wales. The contrast is even greater when the relative sizes of the two populations are taken into account. Why such a disparity in two countries which are geographically close and which show no marked differences in phage types of the bacterium?

A review of various types of evidence by Mark Fielder and colleagues at two London centers, Kingston University and the Health Protection Agency, now indicates likely reasons for the contrast. They highlight in particular the fact that the prevalence of E. coli O157:H7 is largely dependent on season, with greater fecal shedding in warmer seasons. This is directly reflected in more infections.

"Weather differences may be a contributing factor to E. coli O157:H7 geographical variations," Fielder and his coworkers write in Environmental Microbiology (12:2633, 2010). "Scotland on average has greater rainfall, less sunshine and lower temperatures than England and Wales. It has been reported that rainfall can contaminate the surrounding areas and infect individuals subsequently using these areas. Therefore, weather differences, especially in the summer, may be a contributing factor to the difference in E. coli infection rates."

Greater numbers of barbeques, picnics, school trips, and farm visits during the warmer months might be relevant too. Another contributory cause discussed by the Kingston team is the much larger number of people in Scotland dependent on private sources of water. These are supplies, not provided by a company, that come from springs, wells, ponds, lakes, streams, and rivers. Previous reports have shown that they can be a source of E. coli O157:H7.

Seasonality was the main feature to emerge strongly from the second recent study, a survey of the occurrence of Campylobacter jejuni and Campylobacter coli in a river and its related delta, marshes, and sea, in a heavily populated area of northeast Spain. Two surprises here. Firstly, this was the first published report on the presence and levels of thermotolerant Campylobacter species in surface waters in a Mediterranean area. Secondly, while the organisms proved to be widely distributed, there was a pronounced seasonal distribution of the pathogen- but not of fecal indicators.

"This may be because the occurrence of the Campylobacter species, as well as their concentration, may depend not only on different contamination sources and on their contribution to superficial water pollution, but also upon the pathogen's ability to survive, which seems to be related to the climatic conditions of the given geographical area much more than to fecal indicators," the University of Barcelona investigators write (S. Rodriguez and R. Araujo, J. Appl. Microbiol. 109:1027, 2010).

There could be considerably more for us still to learn about the influence of weather and climate on both global and local patterns of infectious disease.