Variation in diazotrophic community structure in forest soils reflects land use history
Introduction
Nitrogen in most forest soils is provided by the decomposition of organic material, inputs from atmospheric deposition, and by microbial nitrogen fixation (Widmer et al., 1999, Nadelhoffer, 2001). In most cases, nitrogen fixation represents a significant contribution to the net nitrogen input in forest soils (Johnson and Curtis, 2001). Nitrogen-fixing, or diazotrophic, microorganisms represent a physiological group of highly specialized Bacteria and Archaea that have a significant functional role in the input of nitrogen to both terrestrial and aquatic environments. The known diversity of diazotrophic microorganisms continues to grow as DNA and mRNA inventories of nifH, the gene that encodes nitrogenase reductase, are expanded and catalogued in databases such as Genbank (Zehr et al., 2003b, Martensson et al., 2009). Although nifH expression is ubiquitous in forest soils (Mergel et al., 2001), the reported diversity of diazotrophs varies dramatically between soils, and such differences in diversity can be used as an indicator of community response to a disturbance (Yeager et al., 2005).
Human activities, particularly those associated with forest management, alter the supply of nutrients in forest ecosystems (Foster et al., 1998, Compton and Boone, 2000, Johnson and Curtis, 2001, Gulledge et al., 2004, Johnson et al., 2005). In the case of the nitrogen cycle, particularly nitrogen fixation, widespread disturbances such as land-use change in the form of clear-cutting can significantly alter diazotrophic populations (Widmer et al., 1999, Shaffer et al., 2000, Johnson et al., 2005, Yeager et al., 2005). Other disturbances, such as chronic N fertilization, have been noted to have an impact on nitrogen-fixing populations in soils of Harvard Forest in Massachusetts (Compton et al., 2004, Gulledge et al., 2004). However, little work has been performed to assess the long-term permanence of such effects, particularly in relation to the long-lasting effect of previous agricultural activity on forest soil diazotrophs.
Old-field succession following abandonment after extended periods of agricultural activity, or secondary growth, is commonly found in the northeastern United States (Compton and Boone, 2000). Overall, very few long-term studies that allow an effective test of the resilience of forest soil diazotroph communities exist. Thus, long-term community responses to disturbance must be inferred from current manipulations or historical reconstruction (Compton and Boone, 2000). Cadwell Memorial Forest in Pelham, Massachusetts, is an excellent research site to study the long-term effect of agricultural activity on secondary-growth forest soils and to examine the resilience of the soil diazotroph community to such a disturbance. After being cleared for agricultural activities between 1783 and the 1850s, these sites were abandoned and allowed to return to forest ecosystems (D'Amato et al., 2005). In 1953, the University of Massachusetts, Amherst acquired the land. The boundaries between old forest sites and secondary-growth sites cleared for agricultural use remain delineated, making it possible to obtain comparative samples to assess microbial community composition under both management histories. Long-term secondary growth should promote homogenous plant–microbe and soil–microbe interactions on both sides of the boundaries. We therefore hypothesized that, after more than a century after the cessation of agricultural activities, few differences in diazotrophic community composition and activity should be observed in forest soils with different land-use history.
In the work presented here we aim to address the question of whether extensive land-use changes such as forest clearing and agricultural activity that occurred more than a century ago have a legacy effect on contemporary forest soil community diversity and function. For this purpose, we have compared the structure of nitrogen-fixing populations and their respective nitrogenase activity in old forest sites with that of adjacent, historically farmed secondary-growth sites.
Section snippets
Soil sampling and analyses
Cadwell Memorial Forest is located in the central hardwood region of southern New England (42°21′ 47″ N, 72°26′ 17″ W) in the towns of Belchertown and Pelham, Massachusetts. The University of Massachusetts, Amherst, has managed the 468 ha of experimental forest since 1951 (Wilson and McComb, 2005). In terms of prior pastureland utilization, during the early to mid 1800s, ten farms operated in this area along with a sawmill and a small woodworking shop (D'Amato et al., 2005). Current vegetation
Chemical and biological properties of forest soils under different management history
Soils from all six sites exhibited very similar chemical characteristics. No significant differences were detected in pH, organic matter content, or the concentration of total phosphorus or nitrogen species across sampling sites or between treatment histories (Table 1). In both sets of treatments, NH4+-nitrogen represented a high proportion (∼95%) of the detected inorganic nitrogen in Cadwell forest soils. Cadwell secondary growth sites (CA sites), however, exhibited significantly higher
Discussion
Agricultural practices have been recognized to have an effect on nitrogen-fixing populations in soil (Yeager et al., 2005, Patra et al., 2006, Orr et al., 2011), but the vast majority of evidence to support this statement has been assessed immediately after the disturbance. Conversely, very little is known about the long-term responses to such disturbance. In preparation for this study, we hypothesized that after over a century of secondary growth, very few differences should be observed in
Acknowledgments
We thank Dr. Matthew Kelty and Dr. Anthony D'Amato for useful discussions about Cadwell Memorial Forest, Sara Izquierdo for help in the acquisition of Cadwell Forest aerial photography, and Jim Krupa for valuable technical assistance. We are also thankful for funding provided by a USDA McIntire-Stennis grant to K.N. and a Lotta M. Crabtree Fellowship awarded to J.A.I.
References (43)
- et al.
Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest
Forest Ecology and Management
(2004) - et al.
Contamination of diverse nifH and nifH-like DNA into commercial PCR primers
FEMS Microbiology Letters
(2005) - et al.
Effects of long-term nitrogen fertilization on the uptake kinetics of atmospheric methane in temperate forest soils
FEMS Microbiology Ecology
(2004) - et al.
Effects of forest management on soil C and N storage: meta analysis
Forest Ecology and Management
(2001) - et al.
The effects of wildfire, salvage logging, and post-fire N-fixation on the nutrient budgets of a Sierran forest
Forest Ecology and Management
(2005) - et al.
Relative abundance of denitrifying and dinitrogen-fixing bacteria in layers of a forest soil
FEMS Microbiology Ecology
(2001) The impacts of nitrogen deposition on forest ecosystems
- et al.
Isolation and gene quantification of heterotrophic N2-fixing bacterioplankton in the Baltic Sea
Environmental Microbiology
(2007) - et al.
The structure of microbial communities in soil and the lasting impact of cultivation
Microbial Ecology
(2001) - et al.
Effects of model root exudates on structure and activity of a soil diazotroph community
Environmental Microbiology
(2005)
New molecular screening tools for analysis of free-living diazotrophs in soil
Applied and Environmental Microbiology
Cloning, DNA sequencing, and characterization of a nifD-homologous gene from the archaeon Methanosarcina barkeri 227 which resembles nifD1 from the eubacterium Clostridium pasteurianum
Journal of Bacteriology
Long-term impacts of agriculture on soil carbon and nitrogen in New England forests
Ecology
Cadwell Forest Management Plan
Polymerase chain reaction denaturing gradient gel electrophoresis analysis of the N2-fixing bacterial diversity in soil under Acacia tortilis ssp. raddiana and Balanites aegyptiaca in the dryland part of Senegal
Environmental Microbiology
Land-use history as long-term broad-scale disturbance: regional forest dynamics in central New England
Ecosystems
Microbial community variation and its relationship with nitrogen mineralization in historically altered forests
Ecology
A global census of nitrogenase diversity
Environmental Microbiology
BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT
Nucleic Acids Symposium Series
Ranking of crop and long-term farming system effects based on soil bacterial genetic profiles
FEMS Microbiology Ecology
Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stand
Environmental Microbiology
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Current address: Department of Biology, Hofstra University, Hempstead, NY 11549, USA.