Drivers of Bacterial Maintenance and Minimal Energy Requirements

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.

Thriving or surviving? Evaluating active microbial guilds in Baltic Sea sediment

“…This agrees with a recent study by Kempes et al . () in which smaller, more energy starved Bacteria focus cellular energy on protein and nucleotide metabolisms, and Orsi et al . () which found that protein cycling accounts for a large percent of cellular activity at low metabolic rates.…”

Microbial community assembly in marine sediments

“…The relationship between community size and energy availability is believed to be the product of a basal power requirement (BPR), which refers to the minimum amount of energy required for basic repair and maintenance functions (Lever et al 2015, Jørgensen & Marshall 2016. Organic matter quality and quantity determine the energy flux available at a given sediment depth and age, and the BPR determines the theoretical upper limit of the community size that can be supported at this energy flux (Hoehler & Jørgensen 2013, Kempes et al 2017. Despite the strong energy limitations in the deep subsurface, amino acid racemization models suggest that vegetative cells must continually turn over their biomass during burial .…”

“…Despite the strong energy limitations in the deep subsurface, amino acid racemization models suggest that vegetative cells must continually turn over their biomass during burial . Active cells may, however, exist in a survival state, devoting their limited energy to the repair and synthesis of essential biomolecules rather than to cell division and growth , Lever et al 2015, Kempes et al 2017.…”

Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time

“…Once dormancy is initiated by starvation or resource limitation (Lennon & Jones, 2011), a cell's metabolism is reserved mostly to essential functions such as biomolecular repair and replacement, rather than to support growth (Kempes et al, 2017;Orcutt et al, 2013;Tijhuis, Van Loosdrecht, & Heijnen, 1993). "Maintenance" energy refers to the sum of the energetic costs of the activities that do not produce growth, but that are required to sustain life.…”