Abstract
Although an existential threat from the microbial world might seem like science fiction, a catastrophic decline in amphibian populations with the extinction of dozens of species has been attributed to a chytrid fungus [1], [2], and North American bats are being decimated by Geomyces destructans, a new fungal pathogen [3]. Hence, individual microbes can cause the extinction of a species. In the foregoing instances, neither fungus had a known relationship with the threatened species; there was neither selection pressure for pathogen attenuation nor effective host defense. Humans are also constantly confronted by new microbial threats as witnessed by the appearance of HIV, SARS coronavirus, and the latest influenza pandemic. While some microbial threats seem to be frequently emerging or re-emerging, others seem to wane or attenuate with time, as exemplified by the decline of rheumatic heart disease [4], the evolution of syphilis from a fulminant to a chronic disease [5], and the disappearance of “English sweating sickness” [6]. A defining feature of infectious diseases is changeability, with change being a function of microbial, host, environmental, and societal changes that together translate into changes in the outcome of a host–microbe interaction. Given that species as varied as amphibians and bats can be threatened with extinction by microbes, the development of predictive tools for identifying microbial threats is both desirable and important.
Highlights
Virulence as an Emergent Property. To those familiar with the concept of emergence (Box 1), it probably comes as no surprise that microbial virulence is an emerging property
The conclusion that virulence is an emergent property is obvious when one considers that microbial virulence can only be expressed in a susceptible host [9]
Intracellular parasitism is associated with genome reduction, a phenomenon that could confer emergent properties, given that deliberate genome reduction in E. coli has led to unexpected emergent properties, such as ease of electroporation and increased stability of cloned DNA and plasmids [14]
Summary
To those familiar with the concept of emergence (Box 1), it probably comes as no surprise that microbial virulence is an emerging property. The traditional view of microbial pathogenesis has been reductionist [7], namely, assigning responsibility for virulence to either the microbe or the host. The outcome of a viral infection can depend on prior infection with related or unrelated viruses that express related antigens; the infection history of a host affects the outcome of subsequent infections [16]. For those accustomed to viewing host– microbe interactions from an evolutionary perspective [17], the emergent nature of virulence is no surprise, for the evolution of life itself can be viewed as an emergent process [18]. Even in relatively well-circumscribed systems such as Darwin’s finches on the Galapagos Islands, evolutionary trends over time became increasingly unpredictable as a consequence of environmental fluctuations [19]
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