Abstract
Microbes maintain themselves through a variety of processes. Several of these processes can be reduced or shut down entirely when resource availability declines. In pure culture conditions with ample substrate supply, a relationship between the maximum growth rate and the energy invested in maintenance has been reported widely. However, at the other end of the resources spectrum, bacteria are so extremely limited by energy that no growth occurs and metabolism is constrained to the most essential functions only. These minimum energy requirements have been called the basal power requirement. While seemingly different from each other, both aspects are likely components of a continuum of regulated maintenance processes. Here, we analyze cross-species tradeoffs in cellular physiology over the range of bacterial size and energy expenditure and determine the contributions to maintenance metabolism at each point along the size-energy spectrum. Furthermore, by exploring the simplest bacteria within this framework– which are most affected by maintenance constraints– we uncover which processes become most limiting. For the smallest species, maintenance metabolism converges on total metabolism, where we predict that maintenance is dominated by the repair of proteins. For larger species the relative costs of protein repair decrease and maintenance metabolism is predicted to be dominated by the repair of RNA components. These results provide new insights into which processes are likely to be regulated in environments that are extremely limited by energy.
Highlights
Understanding the minimal energetic requirements for bacteria has far-reaching importance ranging from estimating total carbon budgets in the deep ocean to understanding the constraints on the origination, survival, and proliferation of life on our own planet and other planetary bodies
We show that comparing the size dependence of total and maintenance metabolism predicts a lower bound on bacterial size consistent with several recent studies (Kempes et al, 2012, 2016)
Our results suggest that at the lowest cell sizes and metabolic rates the cost of maintenance is significant and largely dominated by the cost of repairing proteins
Summary
Understanding the minimal energetic requirements for bacteria has far-reaching importance ranging from estimating total carbon budgets in the deep ocean to understanding the constraints on the origination, survival, and proliferation of life on our own planet and other planetary bodies. We consider systematic trends in cellular physiology that have recently been described empirically and, in some cases, theoretically, for processes spanning the gamut from metabolic rate to protein abundance (Makarieva et al, 2005, 2008; DeLong et al, 2010; Kempes et al, 2012, 2016; Lynch and Marinov, 2015). Our goal is to understand how the detailed processes of a cell, and their differences across species and cell sizes (DeLong et al, 2010; Kempes et al, 2012, 2016; Lynch and Marinov, 2015), contribute to maintenance metabolism. We consider the energetic costs of protein repair, RNA repair, trans-membrane proton gradients, and motility, each as a function of cell size
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