On maintenance and metabolisms in soil microbial communities

Abstract

Biochemistry is an essential yet often undervalued aspect of soil ecology, especially in soil C cycling. We assume based on tradition, intuition or hope that the complexity of biochemistry is confined to the microscopic world, and can be ignored when dealing with whole soil systems. This opinion paper draws attention to patterns caused by basic biochemical processes that permeate the world of ecosystem processes. From these patterns, we can estimate activities of the biochemical reactions of the central C metabolic network and gain insights into the ecophysiology of microbial biosynthesis and growth and maintenance energy requirements; important components of Carbon Use Efficiency (CUE).The biochemical pathways used to metabolize glucose vary from soil to soil, with mostly glycolysis in some soils, and pentose phosphate or Entner-Doudoroff pathways in others. However, notwithstanding this metabolic diversity, glucose use efficiency is high and thus substrate use for maintenance energy and overflow respiration is low in these three soils. These results contradict current dogma based on four decades of research in soil ecology. We identify three main shortcomings in our current understanding of substrate use efficiency: 1) in numeric and conceptual models, we lack appreciation of the strategies that microbes employ to quickly reduce energy needs in response to starvation; 2) production of exudates and microbial turnover affect whole-soil CUE more than variation in maintenance energy demand; and 3) whether tracer experiments can be used to measure the longterm substrate use efficiency of soil microbial communities depends critically on the ability of nongrowing cells to take up tracer substrates, how biosynthesis responds to these substrates, as well as on how cellular activities scale to the community level.To move the field of soil ecology forward, future research must consider the details of microbial ecophysiology and develop new tools that enable direct measurement of microbial functioning in intact soils. We submit that 13 C metabolic flux analysis is one of those new tools.

Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth

“…At the end of the incubation, stored C was sufficient to completely support basal respiration for 109 – 347 h (depending on the treatment), which could be a crucial resource for withstanding starvation or other stress. Much longer periods would be envisaged if accompanied by strong downregulation of energy use in response to the stress 26 . Thus, the resource buffer provided by storage could help microorganisms in terrestrial ecosystems overcome resource fluctuations and support short-term resistance against environmental disturbance 6 .…”

Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth

“…At the end of the incubation, stored C across the various treatments was sufficient to support 109-347 h of microbial respiration at the CO 2 efflux rate of the zero-C, no-nutrient treatment (i.e., basal respiration). Much longer periods would be envisaged if accompanied by strong downregulation of energy use in response to the stress 28 . Storage could thus be a crucial resource for withstanding starvation or other stress.…”

Quantifying thermal adaptation of soil microbial respiration

“…In simpler microbial communities, such as those we found in the warmest soil temperatures, the summation of the smaller number of species’ individual temperature response curves may have resulted in differences in the measured temperature response parameters. The shift in temperature response within and between the different microbial communities may also reflect changes in the dominant glucose metabolising pathway along the gradient 81 . Large changes in microbial diversity and biomass, not accompanied by large changes in the temperature dependence of respiration, imply that respiration is a universal process whose temperature response is largely independent of community composition and abundance.…”