The physiology and ecological implications of efficient growth

Abstract

The natural habitats of microbes are typically spatially structured with limited resources, so opportunities for unconstrained, balanced growth are rare. In these habitats, selection should favor microbes that are able to use resources most efficiently, that is, microbes that produce the most progeny per unit of resource consumed. On the basis of this assertion, we propose that selection for efficiency is a primary driver of the composition of microbial communities. In this article, we review how the quality and quantity of resources influence the efficiency of heterotrophic growth. A conceptual model proposing innate differences in growth efficiency between oligotrophic and copiotrophic microbes is also provided. We conclude that elucidation of the mechanisms underlying efficient growth will enhance our understanding of the selective pressures shaping microbes and will improve our capacity to manage microbial communities effectively.

Figure 1

The influence of limiting resources on the CUE of K. aerogenes NCTC 418 in chemostat cultures. (a) Allocation of carbon in a glycerol-limited chemostat culture as a function of dilution rate (Herbert, 1976). (b) Variation in CUE related to the steady-state glycerol concentration (calculated from Herbert, 1976). (c) Relationship between CUE and the steady-state limiting resource concentration in glucose-, phosphate- or sulfate-limited conditions (calculated from Neijssel and Tempest, 1976). Curve fitting in all panels was generated using a locally weighted regression algorithm (LOESS) to help visualize trends.

Figure 2

CUE of 10 bacterial species related to the energy content of the organic compound supporting growth (calculated from Linton and Stephenson, 1978). Distinct symbols represent different bacterial species. The heat of combustion of representative organic compounds and an average for bacterial biomass (E. coli (130.2) and M. methylotrophus (132.5), calculated from Cordier et al., 1987) are presented on the x axis.

Figure 3

Proposed model of growth efficiency for distinct bacterial life histories. The efficiency of copiotrophic (solid lines) and oligotrophic (dashed lines) bacteria should be compared on resources with the same energy content (indicated by line color) and at the same limiting resource concentration.