On the shifting balance: the case of Staphylococcus aureus CC398

Abstract

The recent study by L. Price et al. [mBio, 3(1):e00305-11, 2012] demonstrating the human origin of the livestock-associated CC398 Staphylococcus aureus provides an excellent example of how bacterial populations can explore a wide range of potential niches and acquire optimal adaptations for life in alternative hosts. The shifting balance theory proposed by Sewall Wright 80 years ago serves as a perfect model for understanding the observed facts: a possibly large CC398 population optimally positioned on the top of a fitness peak for living in a human host probably began evolving long ago by variation, drift, and migration, until it reached the low fitness edge of a neighboring alternative peak in the fitness landscape, one in a livestock host. The bacterial population then evolved again, moving uphill to reach a novel optimal "top of the peak" position in livestock. In the case of CC398, it is worrisome to think that it might readapt to human hosts without losing fitness in livestock; a double-host-adapted organism could certainly be in an optimal position for increasing its virulence and antibiotic resistance.

FIG 1

Red (human) and green (livestock) mountains represent fitness peaks for S. aureus CC398; the higher CC398 (violet circle) is on the peak, the greater its fitness in the corresponding host. In the first row, when the strain migrates from humans to livestock, the fitness decreases, and low fitness is maintained if the transmission between animals is rare. In the second row, a high density of animals (crowded farming) facilitates up-hill climbing in fitness, until optimal fitness is reached; CC398 is now a livestock-adapted organism. In the third row, CC398 migrates to humans again, but its fitness now is low, and transmission between humans is rare.