The effect of resource history on the functioning of soil microbial communities is maintained across time

Biogeosciences, 8, 1477–1486, 2011 www.biogeosciences.net/8/1477/2011/ doi:10.5194/bg-8-1477-2011 © Author(s) 2011. CC Attribution 3.0 License. Biogeosciences The effect of resource history on the functioning of soil microbial communities is maintained across time A. D. Keiser1 , M. S. Strickland1 , N. Fierer2,3 , and M. A. Bradford1 1 School of Forestry and Environmental Studies, Yale University, New Haven, CT, 06511, USA 2 Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA 3 Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, 80309, USA Received: 28 January 2011 – Published in Biogeosciences Discuss.: 23 February 2011 Revised: 18 May 2011 – Accepted: 25 May 2011 – Published: 9 June 2011 Abstract. Historical resource conditions appear to influence microbial community function. With time, historical influences might diminish as populations respond to the contemporary environment. Alternatively, they may persist given factors such as contrasting genetic potentials for adaptation to a new environment. Using experimental microcosms, we test competing hypotheses that function of distinct soil microbial communities in common environments (H1a ) converge or (H1b ) remain dissimilar over time. Using a 6 × 2 (soil community inoculum × litter environment) full-factorial design, we compare decomposition rates in experimental microcosms containing grass or hardwood litter environments. After 100 days, communities that develop are inoculated into fresh litters and decomposition followed for another 100 days. We repeat this for a third, 100-day period. In each successive, 100-day period, we find higher decomposition rates (i.e. functioning) suggesting communities function better when they have an experimental history of the contemporary environment. Despite these functional gains, differences in decomposition rates among initially distinct communities persist, supporting the hypothesis that dissimilarity is maintained across time. In contrast to function, community composition is more similar following a common, experimental history. We also find that “specialization” on one experimental environment incurs a cost, with loss of function in the alternate environment. For example, experimental history of a grass-litter environment reduced decomposition when communities were inoculated into a hardwoodlitter environment. Our work demonstrates experimentally that despite expectations of fast growth rates, physiological Correspondence to: A. D. Keiser () flexibility and rapid evolution, initial functional differences between microbial communities are maintained across time. These findings question whether microbial dynamics can be omitted from models of ecosystem processes if we are to predict reliably global change effects on biogeochemical cycles. 1 Introduction Soil microbial communities play a pivotal role in ecosystems as drivers of biogeochemical processes, including carbon and nitrogen cycling (Allison and Martiny, 2008; Lauber et al., 2009; Bell et al., 2005; Fierer et al., 2007; Manzoni and Porporato, 2009; McGuire and Treseder, 2010; Wallenstein et al., 2010). How the activities of these communities will respond to environmental change, and hence influence carbon storage and nutrient availability, is an important research question for predicting future ecosystem function (Wallenstein et al., 2010). Given high species richness, fast growth rates, physiological flexibility and rapid evolution, soil microbial communities are traditionally assumed to be functionally similar with regard to broad-physiological processes such as the decomposition of organic carbon (Allison and Martiny, 2008; Schimel, 1995; Green et al., 2008; McGuire and Treseder, 2010). This assumption of similarity underlies the majority of terrestrial ecosystem models and is broadly defined as the ability of different microbial communities to carry out a functional process at a similar rate regardless of differences in composition (Allison and Martiny, 2008; Reed and Martiny, 2007). Despite the expectation of functional similarity, microbial communities display biogeographic patterns generated not only by the contemporary environment (i.e. habitat) but Published by Copernicus Publications on behalf of the European Geosciences Union. 1478 A. D. Keiser et al.: History structures microbial communities also historical factors, such as limited dispersal (Martiny et al., 2006; Ramette and Tiedje, 2007). Biogeographic heterogeneity provides conditions suitable for individuals and communities to adapt to their environment (Holt and Gomulkiewicz, 1997; Gholz et al., 2000; Strickland et al., 2009b). This indicates that the history of any one habitat might shape microbial community function under a new resource environment. To test for such historical effects one can compare ecosystem process rates in a common environment, inoculated with microbial communities sourced from different environments (Ayres et al., 2009; Langenheder and Prosser, 2008; Reed and Martiny, 2007; Strickland et al., 2009a). Using this approach, Strickland et al. (2009a) demonstrated that resource history generated functionally dissimilar communities, with history explaining between 22 and 86 % of variance in the ecosystem process measured. What has not been resolved is whether these historical effects diminish as microbial communities respond to contemporary resource conditions. In other words, it is not apparent whether the communities become functionally more similar across time if exposed to a common environment. Such convergence in function might be expected if communities acclimate or adapt given physiological flexibility and natural selection, respectively. If initially distinct communities do become more functionally similar across time in a common environment then this might minimize the need to include microbial dynamics in predictive ecosystem models (see Allison and Martiny, 2008). We used experimental microcosms, in a common garden design, to test whether initially distinct microbial communities exposed to common environments became more functionally similar (i.e. converge) across time (H1a ) or whether they remained functionally dissimilar (H1b ). Microbial inocula were collected from three, paired hardwood-grassland locations in the southeastern United States and introduced to common litter environments. After 100 days, the communities that developed were used to inoculate fresh litter environments and decomposition followed for another 100 days. We repeated this re-inoculation for a third, 100-day period (Appendix A). In addition to assessing function by measuring litter decomposition (as carbon mineralization rates), we also measured microbial community composition using genomic techniques at the end of the first and third 100-day period. Lastly, reciprocal inoculations were introduced in the third 100-day period. We placed microbial (...truncated)