Modeling Microbial Adaptations to Nutrient Limitation During Litter Decomposition

Abstract

Microbial decomposers face large stoichiometric imbalances when feeding on nutrient-poor plant residues. To meet the challenges of nutrient limitation, microorganisms might: (i) allocate less carbon (C) to growth vs. respiration or excretion (i.e., flexible C-use efficiency, CUE), (ii) produce extracellular enzymes to target compounds that supply the most limiting element, (iii) modify their cellular composition according to the external nutrient availability, and (iv) preferentially retain nutrients at senescence. These four resource use modes can have different consequences on the litter C and nitrogen (N) dynamics–modes that selectively remove C from the system can reduce C storage in soil, whereas modes that delay C mineralization and increase internal N recycling could promote storage of C and N. Since we do not know which modes are dominant in litter decomposers, we cannot predict the fate of C and N released from plant residues, in particular under conditions of microbial nutrient limitation. To address this question, we developed a process-based model of litter decomposition in which these four resource use modes were implemented. We then parameterized the model using ∼80 litter decomposition datasets spanning a broad range of litter qualities. The calibrated model variants were able to capture most of the variability in litter C, N, and lignin fractions during decomposition regardless of which modes were included. This suggests that different modes can lead to similar litter decomposition trajectories (thanks to the multiple alternative resource acquisition pathways), and that identification of dominant modes is not possible using “standard” litter decomposition data (an equifinality problem). Our results thus point to the need of exploring microbial adaptations to nutrient limitation with empirical estimates of microbial traits and to develop models flexible enough to consider a range of hypothesized microbial responses.

Microbial Necromass in Soils—Linking Microbes to Soil Processes and Carbon Turnover

“…In spite of the importance of energy fluxes through the soil systems, thermodynamics have only partly been considered for soil systems (Bosatta and Agren, 1999;Lueders et al, 2004;Harris , 2012;Di Lonardo et al, 2017;Manzoni et al, 2021), but have been applied predominantly to technological, chemical, and biochemical processes, such as the production of proteins, and in order to determine the energy use, heat production, and nutrient requirements (Westerhoff et al, 1982;McCarty, 2007;Xiao and VanBriesen, 2008;Kleerebezem and Van Loosdrecht, 2010). The determination of thermodynamic state variables has been applied to soil or natural organic matter processes only in a handful of cases (Barros and Feijóo, 2003;Barros et al, 2007;Herrmann et al, 2014;Barros et al, 2016;Boye et al, 2018).…”

“…In order to understand C transformation and sequestration in soils, an approach that focuses only on C pools and C storage without considering energy and matter fluxes is too limited (Waring et al, 2020;Manzoni et al, 2021). Soil fertility and many other soil functions depend on the activity of various soil microbial communities and thus on continuous energy and C fluxes through the soil system (Janzen, 2015;Waring et al, 2020;Manzoni et al, 2021). For maintaining microbial diversity and ecosystem functions in soil including C storage, both fluxes and stoichiometry issues need to be considered.…”

Intracellular Storage Reduces Stoichiometric Imbalances in Soil Microbial Biomass – A Theoretical Exploration

“…The main difference with respect to the model by Nev and van den Berg (2017) is that in their case stoichiometric imbalances were reduced by allocating cellular resources to acquisition of the least available nutrients, while in our case, nutrient uptake per se is not regulated and the dynamics of storage provide the required buffering capacity. Despite these differences, the qualitative results are comparable, suggesting that multiple resource use modes can alleviate stoichiometric imbalances (Manzoni et al, 2021).…”

“…Other processes that we have not considered here could reduce stoichiometric imbalances without resulting in C loss, such as flexible allocation to C vs. nutrient acquiring extracellular enzymes (Mooshammer et al, 2014;Wutzler et al, 2017), resulting in degradation of nutrientrich organic matter when C-rich labile substrates are available (also referred to as nutrient mining, Craine et al, 2007). It is also possible that nutrient retention is increased compared to C losses during senescence under nutrient limitation (Manzoni et al, 2021). Moreover, microbes could excrete excess C instead of storing it internally.…”

“…Soil microbes are typically considered a single compartment, without distinction between biomass components involved in metabolic activity and storage components. In most of these models, microbial C:N (and often C:P) ratios are held constant (Manzoni and Porporato, 2009), while in some models, microbial C to nutrient ratios can vary in response to stoichiometric imbalances (Allison, 2012;Fatichi et al, 2019;Manzoni et al, 2021). This allows some effects of storage to be captured at the whole cell or microbial community level, but without explicitly modelling storage dynamics.…”