Variation in diazotrophic community structure in forest soils reflects land use history

https://doi.org/10.1016/j.soilbio.2014.09.017Get rights and content

Highlights

  • Cadwell Forest (MA) was used to compare soils with different land use history.

  • Distribution of nifH gene diversity was analyzed with multiple approaches.

  • Diversity of nitrogen fixers was vastly different between two types of sites.

  • Sites with agricultural history exhibited higher nitrogen fixation activity.

  • Combined activity and diversity point to long-term effect of land use history.

Abstract

Microbial nitrogen fixation is an important source of nitrogen in soils of both old and secondary-growth forests. Considering that many soils, which today support secondary-growth forests were once under cultivation, no studies have examined how this kind of disturbance history affects contemporary populations of nitrogen-fixing microbes in forest soils. In the work presented here, we compare secondary-growth forest sites, which were under cultivation more than 150 years ago, to old-growth forest sites in Cadwell Forest, Massachusetts. For each site, nitrogenase activity was measured and the diversity of the nifH gene pools was examined. Three sites with prior agricultural history exhibited higher nitrogenase activity and were dominated by diazotrophs closely related to the α- and γ-Proteobacteria. In contrast, lower nitrogenase activity and the dominance of the anaerobic Cluster III diazotrophs characterized the three old forest sites. Further analyses of species overlap among all six sites revealed that the diazotrophic composition was closely related to previous management history, with agricultural sites clustering together and separate from old forest sites, independent of the proximity between sites. By specifically targeting one of the main functions of microbial communities in soils, the activity and diversity of nitrogen-fixing microorganisms, this work points to a long-lasting effect of former agricultural activities on secondary-growth forest soils, more than one hundred years after succession.

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)

  • H. Bürgmann et al.

    New molecular screening tools for analysis of free-living diazotrophs in soil

    Applied and Environmental Microbiology

    (2004)
  • Y.T. Chien et al.

    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

    (1994)
  • J.E. Compton et al.

    Long-term impacts of agriculture on soil carbon and nitrogen in New England forests

    Ecology

    (2000)
  • A.W. D'Amato et al.

    Cadwell Forest Management Plan

    (2005)
  • M. Demba-Diallo et al.

    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

    (2004)
  • D.R. Foster et al.

    Land-use history as long-term broad-scale disturbance: regional forest dynamics in central New England

    Ecosystems

    (1998)
  • J.M. Fraterrigo et al.

    Microbial community variation and its relationship with nitrogen mineralization in historically altered forests

    Ecology

    (2006)
  • J.C. Gaby et al.

    A global census of nitrogenase diversity

    Environmental Microbiology

    (2011)
  • T.A. Hall

    BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT

    Nucleic Acids Symposium Series

    (1999)
  • M. Hartmann et al.

    Ranking of crop and long-term farming system effects based on soil bacterial genetic profiles

    FEMS Microbiology Ecology

    (2006)
  • M. Hartmann et al.

    Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stand

    Environmental Microbiology

    (2009)
  • Cited by (12)

    • Revegetation of a degraded karst ecosystem triggers shifts in diazotroph communities (composition, diversity, function and assembly processes)

      2022, Applied Soil Ecology
      Citation Excerpt :

      Xu et al. (2019) observed that soil diazotroph community generally changed from Actinobacteria-dominated to Proteobacteria- dominated along a revegetation chronosequence on the Loess Plateau of China. Izquierdo and Klaus (2015) found that changes in diazotrophic community structure reflected land use history in forest soils. Despite the importance of soil diazotrophs to ecosystem functioning, studies mainly focus on patterns of community composition and diversity of diazotrophs response to environmental changes, while the potential mechanisms of these patterns that governing diazotroph communities remain largely unexplored, especially under revegetation processes in degraded ecosystems.

    • Changes in the biological N<inf>2</inf>-fixation rates and diazotrophic community as vegetation recovers on abandoned farmland in a karst region of China

      2021, Applied Soil Ecology
      Citation Excerpt :

      These results show that nifH can be used as a sensitive bioindicator of diazotroph activity and N cycling in soils (Bürgmann et al., 2004). The nifH may also highlight the legacy effects of N applications during agricultural management of previously forested sites, e.g., as observed by Izquierdo and Nüsslein (2015) on sandy loam soil in a temperate deciduous forest in the northeastern USA. Our first hypothesis was that the BNF rates increase at abandoned sloping cropland sites compared with those at the sloping cropland sites and then decrease as vegetation recovery progressed in the Puding Karst CZO.

    • The diversity and co-occurrence patterns of diazotrophs in the steppes of Inner Mongolia

      2017, Catena
      Citation Excerpt :

      Numerous studies indicate that most microorganisms are not cosmopolitan among habitat types (Lozupone and Knight 2007; Wang et al. 2013a). In terrestrial systems, diazotrophic community size and composition can vary according to soil environments (Izquierdo and Nüsslein 2006), soil types (Collavino et al. 2014), soil use history (Izquierdo and Nüsslein 2015), soil management (Ashok et al. 2006) and vegetation (Junier et al. 2009; Mao et al. 2013). Walker et al. (2008) report that the site is the dominant factor differentiating diazotrophic communities, reflecting the variation in plant community composition, soil characteristics, moisture and temperature that combine to create the unique characteristics of each site.

    View all citing articles on Scopus
    1

    Current address: Department of Biology, Hofstra University, Hempstead, NY 11549, USA.

    View full text