Microbial community structure and abundance in the rhizosphere and bulk soil of a tomato cropping system that includes cover crops

Highlights

• We assessed soil microbial communities in rotational agroecosystems.

• We showed cover crops impact the rhizosphere microbial community of succeeding tomato cash crops.

• qPCR revealed hairy vetch increased soil microbial ribosomal gene # over a no cover crop treatment.

• Phylum-specific primers were used to target community structure changes among five major phyla.

Abstract

Understanding microbial responses to crop rotation and legacy of cropping history can assist in determining how land use management impacts microbially mediated soil processes. In the literature, one finds mixed results when attempting to determine the major environmental and biological controls on soil microbial structure and functionality. The objectives of this research were to: (1) Qualitatively and quantitatively measure seasonal and antecedent soil management effects on the soil microbial community structure in the rhizosphere of a subsequent tomato crop (Solanum lycopersicum) and (2) Determine phylum scale differences between the rhizosphere and bulk soil microbial community as influenced by the antecedent hairy vetch (Vicia villosa), cereal rye (Secale cereale), or black plastic mulch treatments. In this report, we use terminal restriction fragment length polymorphisms in the 16s rDNA gene to characterize changes in microbial community structure in soil samples from a field replicated tomato production system experiment at USDA-ARS Beltsville Agricultural Research Center, Beltsville, MD, USA. We found season of the year had the strongest influence on the soil microbial community structure of some of the major microbial phyla. Although we monitored just a few of the major microbial phyla (four Eubacteria and Archaea), we found that the effects of the tomato plant on the structural composition of these phyla in the rhizosphere differed dependent on the antecedent cover crop. Increased understanding of how agricultural factors influence the soil microbial community structure under field conditions is critical information for farmers and land managers to make decisions when targeting soil ecosystem services that are microbially driven.

Introduction

Soil microbes play critical roles in soil biogeochemistry, soil fertility, and disease ecology (Pace, 1997). Recently, extensive efforts have been made to characterize the differential effects various plant species have on both the structure and function of the soil microbial community (Sorensen et al., 2009, Maul and Drinkwater, 2010). The influence of plants on the soil microbial community can be especially important in agricultural systems in which cash and cover crop selection can vary from short rotations (2-3 years) that might include one or two crop species to longer rotations (6-10 years) which might include six or eight species including both annual and perennial crops (Lundquist et al., 1999, Schomberg et al., 2006, Carrera et al., 2007, Spargo et al., 2011). Understanding plant-microbe responses in the context of crop rotation and legacy of cropping history can assist in determining how land use management and changing climatic conditions impact microbially mediated soil processes.

Many interacting factors drive microbial community structure and function in soil ecosystems at different scales, making it difficult to determine the roles of individual factors, unless scale and ecosystem legacy (e.g., crop rotation, plant species legacy) are taken into consideration. For example, pH may drive soil microbial community structure at the continental scale (Fierer and Jackson, 2006), whereas differences at the regional (Green et al., 2004, Petchey and Gaston, 2009) and local scale may be driven by soil type or soil texture (Buyer et al., 1999, Wieland et al., 2001, Girvan et al., 2003). The dominant drivers of microbial community structure and function may also differ at the plot or sub-plot scale and can be driven by interactions between these larger-scale drivers, plant species, and land use history (Hawkes et al., 2005, Grandy et al., 2009, Maul and Drinkwater, 2010).

Agroecosystems offer excellent models for determining the underlying mechanisms controlling soil microbial community structure. In general, agroecosystems have well-defined histories, known soil types, and are managed in a manner that allows isolation of biological, edaphic, and plant species factors that have been shown to influence soil microbial community structure and function (Frey et al., 1999, Fliessbach and Mader, 2000, Buckley and Schmidt, 2001, Spargo et al., 2011). Determination of factors that influence microbial community composition under field conditions has significant impact on understanding how management affects crop quality, disease ecology, and biogeochemical cycling (Buckley and Schmidt, 2001, Balser and Mary, 2005, Zhou and Everts, 2007, Avrahami and Bohannan, 2009).

Tomatoes and other high-value crops are often grown on raised beds covered with black polyethylene mulch which offers many positive benefits, including rapid soil warming, water conservation, and weed suppression (Teasdale and Abdul-Baki, 1995, University_of_Maryland_Extension_Bulletin_236, 2012). Alternative systems that use cover crops instead of black polyethylene and minimize soil tillage and fossil fuel usage have been developed and tested at the Beltsville Agricultural Research Center (BARC), USA. Beds are formed in the fall and planted with a cover crop. In the spring, the cover crop is mowed and the crop residue left in place. The vegetable seedlings are planted directly through the cover crop residue. Minimum tillage systems modeled on this approach that use winter annual cover crops to conserve soil nitrogen and suppress spring weeds have been shown to improve soil quality while maintaining profitability (AbdulBaki et al., 1997, Abdul-Baki and Teasdale, 2007, Díaz-Pérez et al., 2008).

There are the issues regarding disease control in tomato production systems stimulated by the international phase out of the soil fumigant methyl bromide (Montreal Protocol on Substances that Deplete the Ozone Layer and the Clean Air Act, Jan 1, 2005). Cover cropping in rotation with tomatoes is emerging as a potential alternative to methyl bromide (Gilreath and Santos, 2004, Chellemi et al., 2012, Hansen and Keinath, 2013), but variability in the disease reducing efficacy among cover crop species has caused low rates of adoption among farmers. The work presented here is a step toward determining the specific effects of different cover crops on broad groups within the soil microbial community.

We previously showed, using phospholipid fatty acid analysis (PLFA), that farming systems that employ winter annual cover crops tended to increase microbial biomass of major groups of bacteria, fungi, arbuscular mycorrhizae, and protozoans compared to black polyethylene mulch, although some groups increased more than others. The rhizosphere microbial community of the tomato plant was significantly influenced by the previous rye (Secale cereale) or vetch (Vicia villosa) cover crop species. Structural analysis of the soil microbial community also showed that the soil microbiota in the tomato's rhizosphere were responding more to the antecedent cover crop than to the indirect impact of cover crop or mulch on soil moisture and temperature (Buyer et al., 2010).

The short-term impact of a winter annual cover crop can have legacy effects on cycling of soil nutrients and microbial community structure, and if better understood could help land managers plan crop rotation schedules to target particular ecosystem services. For example, legumes add nitrogen to the soil which can be used by the following cash crop, most Poaceae (grasses) are effective at catching and recycling excess nutrients from a previous phase of the cropping rotation. Bakker et al. (2010) show that plant species diversity and the indirect effects on soil nutrient status influence the suppressive phenotype of soil streptomycetes. In addition, some leguminous cover crop species have recently been reported to suppress plant pathogens such as Fusarium oxysporum (Zhou and Everts, 2007).

The objectives of this research were to: (1) Qualitatively and quantitatively measure seasonal and antecedent soil management effects on the soil microbial community structure in the rhizosphere of a subsequent tomato crop (Solanum lycopersicum) and (2) Determine phylum scale differences between the rhizosphere and bulk soil microbial community as influenced by the antecedent hairy vetch (Vicia villosa), cereal rye (Secale cereale), or black plastic mulch treatments.