Microbial carbon limitation: The need for integrating microorganisms into our understanding of ecosystem carbon cycling

Abstract

Numerous studies have demonstrated that fertilization with nutrients such as nitrogen, phosphorus, and potassium increases plant productivity in both natural and managed ecosystems, demonstrating that primary productivity is nutrient limited in most terrestrial ecosystems. In contrast, it has been demonstrated that heterotrophic microbial communities in soil are primarily limited by organic carbon or energy. While this concept of contrasting limitations, that is, microbial carbon and plant nutrient limitation, is based on strong evidence that we review in this paper, it is often ignored in discussions of ecosystem response to global environment changes. The plant‐centric perspective has equated plant nutrient limitations with those of whole ecosystems, thereby ignoring the important role of the heterotrophs responsible for soil decomposition in driving ecosystem carbon storage. To truly integrate carbon and nutrient cycles in ecosystem science, we must account for the fact that while plant productivity may be nutrient limited, the secondary productivity by heterotrophic communities is inherently carbon limited. Ecosystem carbon cycling integrates the independent physiological responses of its individual components, as well as tightly coupled exchanges between autotrophs and heterotrophs. To the extent that the interacting autotrophic and heterotrophic processes are controlled by organisms that are limited by nutrient versus carbon accessibility, respectively, we propose that ecosystems by definition cannot be ‘limited’ by nutrients or carbon alone. Here, we outline how models aimed at predicting non‐steady state ecosystem responses over time can benefit from dissecting ecosystems into the organismal components and their inherent limitations to better represent plant–microbe interactions in coupled carbon and nutrient models.

Long‐term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems

“…Reduced belowground C allocation by plants may suppress microbial enzyme production due to C and energy limitations of microbial metabolism and growth over time (Mooshammer, Wanek, Zechmeister-Boltenstern, & Richter, 2014;Soong et al, 2019). This explanation is supported by our finding that N loading increases microbial specific phosphatase expression in the short-term, but not in the long-term.…”

“…Thus, it is likely that there is an ecosystem‐specific threshold, above which prolonged N inputs do not exacerbate the P limitation, but instead reduce belowground C allocation (Tian, Wang, Sun, & Niu, 2016). Reduced belowground C allocation by plants may suppress microbial enzyme production due to C and energy limitations of microbial metabolism and growth over time (Mooshammer, Wanek, Zechmeister‐Boltenstern, & Richter, 2014; Soong et al., 2019). This explanation is supported by our finding that N loading increases microbial specific phosphatase expression in the short‐term, but not in the long‐term.…”

Response of Soil Bacterial Community Diversity and Composition to Time, Fertilization, and Plant Species in a Sub-Boreal Climate

“…In contrast, no OTUs separated the control from the synthetic fertilizer treatment. The soil bacterial communities are primarily organic C limited, and only secondarily N limited (Soong et al, 2020), which may explain the similarity of the communities in the control and the synthetic fertilizer treatment. According to the report from Fierer et al (2007), the continuous C input in the organic fertilizer treatment may have contributed to the higher abundances of the copiotrophic Bacteroidetes OTUs.…”

“…With elevated N input or across a N gradient, the community composition became progressively more distinct at higher N levels from those at no or lower levels of N fertilizer (Ramirez et al, 2010;Fierer et al, 2012). In addition, Soong et al (2020) reported that soil organic carbon (C) content is the primary limitation for heterotrophic microbial communities.…”

Fungal Community, Not Substrate Quality, Drives Soil Microbial Function in Northeastern U.S. Temperate Forests

“…Instead, in this study, we observed a strong positive correlation between EcM relative abundance and free-living microbial CUE. This positive response could have been driven by considerable EcM exudate secretion to the surrounding microbial community (Phillips and Fahey, 2006;Frey, 2019), outweighing the potential negative effects of nutrient competition between the free-living community and EcM (Phillips and Fahey, 2005;Fransson et al, 2016;Soong et al, 2020). This mechanism is further supported by a study which found that EcM exudate production decreased under elevated soil N conditions, followed by a decrease in microbial growth and biomass (Gorka et al, 2019).…”