Effects of initial microbial biomass abundance on respiration during pine litter decomposition

RESEARCH ARTICLE Effects of initial microbial biomass abundance on respiration during pine litter decomposition Michaeline B. N. Albright ID1*, Andreas Runde1, Deanna Lopez1, Jason Gans1, Sanna Sevanto2, Dominic Woolf3, John Dunbar1 1 Bioscience Division, Los Alamos National Laboratory, Los Alamos, NM, United States of America, 2 Earth and Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM, United States of America, 3 College of Agriculture and Life Sciences, Cornell University, Ithaca, NY, United States of America a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Albright MBN, Runde A, Lopez D, Gans J, Sevanto S, Woolf D, et al. (2020) Effects of initial microbial biomass abundance on respiration during pine litter decomposition. PLoS ONE 15(2): e0224641. https://doi.org/10.1371/journal. pone.0224641 Editor: Riikka Rinnan, University of Copenhagen, DENMARK Received: October 15, 2019 Accepted: January 23, 2020 Published: February 14, 2020 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0224641 Copyright: © 2020 Albright et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Unprocessed sequences are available through NCBI’s Sequence Read Archive (PRJNA601499) * Abstract Microbial biomass is increasingly used to predict respiration in soil organic carbon (SOC) models. Its increased use combined with the difficulty of accurately measuring this variable points a need to directly assess the importance of microbial biomass abundance for carbon (C) cycling. To test the hypothesis that the initial microbial biomass abundance (i.e. biomass abundance on new plant litter) is a strong driver of plant litter C cycling, we manipulated biomass abundance by 10 and 100-fold dilution and composition using 12 source communities on sterile pine litter and measured respiration in microcosms for 30 days. In the first two days of microbial growth on fresh litter, a 100-fold difference in initial biomass abundance caused an average difference in respiration of nearly 300%, but the effect rapidly declined to less than 30% in 10 days and to 14% in 30 days. Parallel simulations with a soil carbon model, SOMIC 1.0, also predicted a 14% difference over 30 days, consistent with the experimental results. Model simulations predicted convergence of cumulative CO2 to within 10% in three months and within 4% in three years. Rapid microbial growth, evidenced by appearance of visible microbial mats on the litter during the first week of incubation, likely attenuates the effects of large initial differences in biomass abundance. In contrast, the persistence of source community as an explanatory factor in driving differences in respiration across microcosms supports the importance of microbial composition in C cycling. Overall, the results suggest that the initial abundance of microbial biomass on litter is a weak driver of C flux from litter decomposition over long timescales (months to years) when litter communities have equal nutrient availability. By extension, slight variation in the timing of microbial dispersal to fresh litter is likely to be a minor factor in long-term C flux. Importance Microbial biomass is one of the most common microbial parameters used in land carbon (C) cycle models, however, it is notoriously difficult to measure accurately. To understand the consequences of mismeasurement, as well as the broader importance of microbial biomass abundance as a direct driver of ecological phenomena, greater quantitative understanding of the role of microbial biomass abundance in environmental processes is needed. Using PLOS ONE | https://doi.org/10.1371/journal.pone.0224641 February 14, 2020 1 / 19 Effects of initial microbial biomass on decomposition Funding: This work was supported by the U.S. Department of Energy, Office of Science, Biological and Environmental Research Division, under award number F260LANL2018 to JD. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. microcosms, we manipulated the initial biomass of numerous microbial communities across a 100-fold range and measured effects on CO2 production during plant litter decomposition. We found that the effects of initial biomass abundance on CO2 production was largely attenuated within a week, while the effects of community type remained significant over the course of the experiment. Overall, our results suggest that initial microbial biomass abundance in litter decomposition within an ecosystem is a weak driver of long-term C cycling dynamics. Introduction Microbial decomposition of plant litter is a key process in terrestrial carbon (C) cycling [1]. Although the dynamics of plant litter decomposition have been studied for decades [2], accurate prediction of ecosystem CO2 fluxes remains a challenge because the controls on decomposition and their response to climate change are not fully understood [3]. Whereas early SOC models focused mostly on abiotic controls (e.g. substrate, moisture, and temperature) [4], an emerging body of research suggests that microbial factors play a key role in regulating decomposition [5–7]. General microbial abundance in soil is a common microbial property incorporated in SOC models as a factor affecting the rate of decomposition of various organic carbon pools [8, 9]. In models, biomass abundance is typically not measured but, rather, computed as a state variable whose dynamic size is determined by an interaction between the model’s structure and parameters, and environmental conditions such as climate, soil physical and chemical properties, and organic matter additions [3, 8]. Microbial biomass is estimated in this fashion in part because of the cost and logistical barriers to measuring microbial biomass in soils globally. Field studies that have measured soil microbial biomass abundance show that it changes over space and time [10], and in response to changing climate [11–13] or disturbance [14]. Measurements of microbial biomass in soils across the globe range from fractions of a gram to 250 grams of biomass C per m2 [15]. Biomass abundance is thought to be largely controlled by organic substrate and moisture availability [11, 16, 17]. Although microbial biomass is an established factor in SOC models, its relative importance as a driver of variation in soil C cycling is an ongoing question, e (...truncated)