Soil Biology & Biochemistry
Soil Microbial Communities and Function in Alternative Systems to Continuous Cotton V. Acosta-Martínez* G. Burow T. M. Zobeck USDA-ARS Cropping Systems Research Lab. Lubbock, TX 79415
V. G. Allen Dep. of Plant and Soil Science Texas Tech Univ. Lubbock, TX 79409
Cotton (Gossypium hirsutum L.) monoculture under conventional tillage has been the predominant cropping system in the Southern High Plains region of the United States since the 1940s. This study evaluated other cropping systems and land uses for their potential to increase soil quality and enhance soil functioning compared with continuous cotton (Ct-Ct), including a mixture of grasses in the Conservation Reserve Program (CRP), a pasture monoculture [Bothriochloa bladhii (Retz) S.T. Blake] and a cotton–winter wheat (Triticum aestivum L.)– corn (Zea mays L.) rotation (Ct-W-Cr). Soil microbial communities were evaluated according to microbial biomass C (MBC) and N (MBN), fatty acid methyl ester (FAME) profiling, and molecular cloning techniques. Soil MBC was higher under the alternative systems at 0 to 5 cm (CRP > pasture = Ct-W-Cr > Ct-Ct), 5 to 10 cm (CRP = Ct-W-Cr > pasture > Ct-Ct), and 10 to 20 cm (CRP = pasture = Ct-W-Cr > Ct-Ct). Soil DNA concentration was correlated with key soil quality parameters such as microbial biomass (r > 0.52, P < 0.05), total C (r = 0.372, P < 0.1), and total N (r = 0.449, P < 0.05). The 16S rRNA gene banding patterns (0–5 cm) of undisturbed systems (CRP and pasture) were more similar to each other than to Ct-Ct and Ct-W-Cr. Fungal/bacterial FAME ratios were higher under CRP and pasture than under Ct-Ct at 0 to 5 and 5 to 10 cm. This study found increases in sensitive soil quality parameters under alternative management compared with cotton monoculture. Abbreviations: CRP, Conservation Reserve Program; Ct-Ct, continuous cotton; Ct-W-Cr, cotton– wheat–corn rotation; FAME, fatty acid methyl ester; MB, microbial biomass; MBC, microbial biomass carbon; MBN, microbial biomass nitrogen; PCA, principal components analysis; PCR, polymerase chain reaction.
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n the semiarid High Plains region of the United States, the typical practice since the 1940s is cotton monoculture under conventional tillage, which has provided low levels of organic inputs compared with crop rotations that include diverse crops under no-till management in humid regions (Moore et al., 2000; Acosta-Martínez et al., 2004; Allen et al., 2008). Irrigated cotton production in this region has provided high economic profit at the expense of high water use that has exceeded the recharge potential of the Ogallala aquifer in this lowrainfall region. Today, regional challenges imposed by the impending loss of the Ogallala aquifer for irrigation, high soil erosion, and stressful climatic conditions have prompted producers to reconsider their options, as past successes are at risk. Alternative management in this region includes the conversion of continuous cotton land to the CRP, perennial pastures, or cotton rotations with other crops. Several efforts to evaluate the sustainability of alternative management for this region are taking place (Texas Alliance for Water Conservation, 2007; Allen et al., 2008), but little is known about how alternative management practices might impact soil quality compared with the typical practice of continuous monoculture cotton. Microbial communities are important to soil quality and functioning because they control the potential for enzyme (i.e., hydrolases)-mediated substrate catalysis (Kandeler et al., 1996), which drives biogeochemical cycles. Thus, understanding the changes in the size, composition, and activity of soil microbial communities following implementation of various land use and Soil Sci. Soc. Am. J. 74:1181–1192 Published online 21 May 2010 doi:10.2136/sssaj2008.0065 Received 27 Feb. 2008. *Corresponding author (
[email protected]). © Soil Science Society of America, 5585 Guilford Rd., Madison WI 53711 USA All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.
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management systems is an important component in selecting management practices to improve ecosystem services, such as nutrient cycling and C sequestration. The CRP was initiated in the United States in 1985 to return eroded land to grass and forest vegetation. The CRP is the largest environmental program administered by the USDA, with enrollment exceeding 13.8 Mha across all 50 states including Texas, where almost 1.62 Mha or 17,750 farms are enrolled (Allen and Vandever, 2005). Several benefits have been recognized for the CRP, including increased wildlife populations, reduced water runoff and sedimentation, and protection of water sources (i.e., groundwater, lakes, and streams). More recently, the benefits for soil quality under the CRP have been recognized (Staben et al., 1997; Acosta-Martínez et al., 2003, 2008; Bronson et al., 2004). The effectiveness of this program in achieving soil quality improvements has not been thoroughly evaluated in the High Plains region, however, where about 1 Mha covered under CRP contracts expired at the end of 2009 (NRCS, 2008). Previous studies in sandy soils from the High Plains showed no significant differences in total C under CRP compared with tilled cotton systems after 10 yr, but higher soil enzyme activities were detected under the CRP (Acosta-Martínez et al., 2003; Bronson et al., 2004). More information is needed, however, to evaluate the effects of the CRP on sensitive soil quality parameters such as microbial communities and the metabolic potential of soil as indicated by enzyme activities. Integrating perennial pasture into the whole farming system is an option that has been adopted quickly throughout the High Plains region for integrated cotton and livestock production systems (Allen et al., 2005, 2008; Philipp et al., 2005). Allen et al. (2008) found that integration of cotton and livestock grazing not only reduces water use by 23%, but could also yield higher profits than continuous cotton. Previous studies have reported that changing cropland to perennial grassland can lead to increases in C sequestration, and thus in soil aggregate stability and microbial biomass and activity (Karlen et al., 1999; Potter et al., 1999; Acosta-Martínez et al., 2004). Crop rotations have also been reported to exert a significant influence on soil quality because crop residues are the primary source of organic matter (Campbell et al., 1991). Cotton rotations with other crops such as corn or wheat have been implemented in the northern part of the High Plains region, which has higher precipitation than the southern part of this region. It is not known, however, how the recently implemented cotton rotations or pastures have affected the microbial communities and metabolic functioning of soil compared with continuous monoculture cotton and CRP land in the High Plains region. Characterization of soil microbial community structure has been possible by assessing fatty acids or nucleic acids derived from microbial cells. Using the FAME method, specific fatty acids have been proposed as biomarkers to broad taxonomic microbial groups. For example, fungal populations have been evaluated using suggested fungal FAME biomarkers such as 18:2ω6c and 18:3ω6c (Frostegård et al., 1993) and arbuscular fungal mycor1182
rhiza indicators such as 18:1ω9c and 16:1ω5c (Olsson, 1999; Madan et al., 2002). The FAME marker 20:4ω6c has been suggested for the evaluation of protozoan abundance (Walling et al., 1996). The relative abundance of bacterial populations has been determined in soil with several FAMEs for Gram-positive (G+) bacteria (a15:0, i15:0, i16:0, a17:0, and i17:0), Gram-negative (G−) bacteria (13:0 2OH, 13:0 3OH, and cy17:0), and actinomycetes (10Me 16:0, 10Me 17:0, and 10Me 18:0), as suggested by previous studies (Wright, 1983; Kroppenstedt, 1992; Walling et al., 1996; Zelles, 1997). Although FAME analysis provides general information about the soil microbial community composition and broad taxonomic information, it does not provide information at the species level. Recent studies reported that 16S rRNA can provide bacterial fingerprint patterns related to pollution ( Joynt et al., 2006), manure applications (Sun et al., 2004), and land uses (Upchurch et al., 2008; Wu et al., 2008). The 16S rRNA technique has opened numerous opportunities to better understand the microbial community structure of soils because bacteria are the most abundant and diverse group of soil organisms, with estimates of 104 to 106 distinct genomes per gram of soil (Vestal and White, 1989; Gans et al., 2005). Results from both bacterial FAME indicators and 16S rRNA analyses will provide better understanding of the impacts of management and land use on bacterial populations. Changes in microbial communities may lead to changes in the metabolic capacity of soils, as indicated by the activities of soil enzymes, which can be determined with simple analyses that require low labor costs compared with other biochemical analyses (Ndiaye et al., 2000). Enzyme activities have been reported to be sensitive indicators of changes in soil quality (Klose et al., 1999; Moore et al., 2000; Ndiaye et al., 2000; Trasar-Cepeda et al., 2000). The first objective of this study was to determine the microbial biomass C and N and the community structure using both FAME analysis and 16S rRNA gene banding patterns and sequences of bacterial populations in a typical soil of the High Plains region under continuous Ct-Ct compared with a Ct-WCr rotation and two undisturbed systems: CRP land and a perennial pasture. Our second objective was to explore the relationship of the microbial community structure as affected by management with soil metabolic functioning by measuring enzyme activities involved in C (β-glucosaminidase, β-glucosidase, and α-galactosidase), N (β-glucosaminidase), P (alkaline phosphatase), and S (arylsulfatase) nutrient transformations and cycling.
MATERIALS AND METHODS Experimental Design and Soil Sampling This study was conducted at the Texas Alliance for Water Conservation (TAWC) field study covering 1619 ha in the Texas High Plains region. The TAWC field study involves 26 producer farms and nearby undisturbed areas. Sites within this field study are distributed within Hale County (center point: 34°5ˇ N, 101°50ˇ W) and Floyd County (center point: 34°5ˇ N, 101°20ˇ W). The elevation of these counties ranges from 2600 to 3600 ft above sea level. Temperatures range in January from an average low of 4°C to an average high of 12°C,
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and in July from 19 to 34°C. The average annual rainfall is 483 mm, of which 279 mm is received as snowfall. We selected sites under a Pullman clay loam soil with 38% clay and 34% sand (McMichael and Lascano, 2003) and studied three representative sites for each system (CRP, pasture, Ct-W-Cr, and Ct-Ct). The sites’ size ranged from 11.5 ha (one of the Ct-W-Cr sites) to 89.9 ha (one of the pasture sites). Before conversion to CRP, pasture, and Ct-W-Cr rotations, the soils of this region had been primarily under continuous cotton monoculture since 1940. A detailed description of the size of the sites, crop cultivars, and management applied on these systems was given in Texas Alliance for Water Conservation (2007). In brief, the CRP sites have not been disturbed, irrigated, or fertilized since their establishment (at least 10 yr). These sites were established under a diverse mixture of grasses typical of this region (‘WW-Spar’ Old World bluestem [Bothriochloa ischaemum (L.) Keng. var. ischaemum (Hack.)], blue grama [Bouteloua gracilis (Willd. ex Kunth) Lag. ex Griffiths], and green sprangletop [Leptochloa dubia (Kunth) Nees]). Pasture sites were established under a monoculture of ‘WW-B. Dahl’ Old World bluestem [Bothriochloa bladhii (Retz) S.T. Blake] that was irrigated with a center pivot for at least 3 yr before sampling time. The sites under Ct-Ct and Ct-W-Cr were conventionally tilled every autumn to 15-cm depth. The Ct-W-Cr rotation sites were established for at least 3 yr at the time of sampling under center pivot irrigation. For this rotation, cotton was planted at a 76.2-cm row spacing, corn was generally grown from April to August with a 50.8-cm row spacing, and winter wheat was planted in the autumn following cotton harvest. Cotton was generally planted during May at the agricultural sites. All irrigated sites received between 127 and 508 mm of water, depending on the year, to provide the minimum irrigation received in this region. Continuous cotton sites were unirrigated (dryland) and cotton was planted at 102-cm row spacing. Soil samples were collected in February 2006 at 0- to 5-, 5- to 10-, and 10- to 15-cm depths from the three sites available as field replicates for each system. A completely randomized approach was used to identify three sampling locations per site (with 50 m of separation). Thus, a total of nine samples were taken to represent each system. Each soil sample was a composite mixture of four subsamples taken within a 0.25-m radius. The soil samples were sieved to Ct-Ct) and MBN (pasture = Ct-W-Cr > CRP > Ct-Ct) than under Ct-Ct at the 0- to 5-cm depth (Fig. 1a and 1b). In addition, soil MBC was higher under the alternative systems compared with Ct-Ct at 5- to 10- and 10- to 20-cm SSSAJ: Volume 74: Number 4 • July–August 2010
depths. Soil MBN was also higher under the alternative systems at 5 to 10 cm, but was only higher under pasture than under CtCt at 10 to 20 cm. Soil MBC was correlated with total C (r = 0.851, P < 0.001) and total N (r = 0.855, P < 0.001), but correlations between MBN and total C or total N were not significant because MBN was lower in the soil under CRP than under pasture or Ct-W-Cr. The soil DNA concentration was higher under pasture and CRP than Ct-Ct at 0 to 5 cm and similar under Ct-W-Cr and Ct-Ct (Fig. 1c). There was a higher DNA concentration at 0 to 5 cm than 5 to 10 cm for the undisturbed systems (CRP and pasture [P < 0.05]), while there were no differences in DNA concentration with depth for the Ct-W-Cr and Ct-Ct systems due to soil mixing with the tillage operations. The soil DNA concentration was correlated with soil quality measurements related to soil C and N pools such as MBC (r = 0.520, P < 0.01), MBN (r = 0.528, P < 0.01), total C (r = 0.372, P < 0.1), and total N (r = 0.449, P < 0.05) for the two soil depths evaluated.
Microbial Community Structure An ANOVA for total FAMEs area showed significant system (P < 0.001) and depth (P < 0.01) effects (Table 1). Total FAMEs area was higher under CRP and Ct-W-Cr than Ct-Ct at all soil depths. Total FAMEs area was correlated with the MBC results for each depth (r = 0.45–0.58, P < 0.01 to Ct-W-Cr > Ct-Ct) only at the 0- to 5-cm depth. Therefore, it is possible that there were no major differences in cellulose degradation at lower soil depths (5–10 and 10–20 cm) among the systems. It has been acknowledged that fungal and bacterial populations play different roles in decomposition processes in soil (Bailey et al., 2002), but to our knowledge there is limited information relating microbial community structure to metabolic function indicated by enzyme activities as affected by soil management. Our study documents changes in both bacterial and fungal populations that are consistent with the higher enzyme activities under CRP land, pasture, and the Ct-W-Cr rotation compared with Ct-Ct. The higher fungal/bacterial ratios and enzyme activities under CRP land and pasture compared with Ct-W-Cr and Ct-Ct suggest a significant contribution of fungal populations to the metabolic function of undisturbed soils. The higher enzyme activities found under Ct-W-Cr than Ct-Ct can also be attributed to the differences in microbial community structure found between these systems. For example, while both systems (Ct-W-Cr and Ct-Ct) had a more bacterial-dominated microbial community structure compared with the CRP land and pasture according to the fungal/bacterial ratios in the PCA plots, the fungal and bacterial FAMEs were higher under Ct-WCr than Ct-Ct at all soil depths. Our findings agree with previous suggestions of the significant role of fungal populations in the synthesis and ecological role of extracellular enzymes that participate in the degradation of chitin (i.e., β-glucosaminidase) and cellulose (i.e., cellulose and β-glucosidase; Miller et al., 1998; Parham and Deng, 2000). Our results from 16S rRNA analysis also distinguished bacteria (i.e., Actinobacteria) in the soil under the CRP land and pasture that may be involved in the increased enzyme activities SSSAJ: Volume 74: Number 4 • July–August 2010
of the undisturbed systems compared with Ct-Ct. Actinobacteria have been recognized for their role in the decomposition of cellulose and chitin, and thereby contribute to soil organic matter turnover and C cycling (Acosta-Martínez et al., 2008). Acosta-Martínez et al. (2008) found further differences in the soil bacterial communities among these systems using pyrosequencing, including higher Bacteroidetes under Ct-Ct than the alternative systems. In addition, they also reported the lowest bacterial diversity indices under Ct-Ct, intermediate under the undisturbed CRP and pasture systems, and the highest under the Ct-W-Cr rotation. Management can also have varying effects on the different pools of an enzyme in the soil, which include the intracellular (inside active microbial cells) and extracellular (in the soil solution or attached to soil surfaces) enzyme fractions (Klose et al., 1999; Nannipieri et al., 2002). This may explain the different response of the soil MB and enzyme activities found in this study for pasture and CRP land. For example, the soil under the CRP showed higher MBC (but also lower MBN and DNA concentration) compared with the pasture soil, but the pasture soil was still able to sustain similar levels of enzyme activities to CRP after only 3 yr.
CONCLUSIONS This study documents the effectiveness of the CRP after 10 yr in achieving soil quality improvements in land that was previously under continuous cotton in the semiarid region of the Southern High Plains. The conversion of a clay loam soil under Ct-Ct to the CRP led to increases in total C and MB, shifts in microbial community structure to higher fungal/bacterial ratios, and increased enzyme activities after 10 yr. Although the pasture had been established for only 3 yr, similar activity levels of β-glucosaminidase, arylsulfatase, and alkaline phosphatase were found in the CRP land (under a diverse mixture of grasses) and pasture (under a monoculture of Old World bluestem) at the 0- to 20-cm depth. Moreover, significant changes in microbial communities and the metabolic potential of the soil as indicated by enzyme activities were detected under a crop rotation that included diverse crops (Ct-W-Cr) compared with Ct-Ct after only 3 yr. The positive soil microbial responses detected under the CRP land, pasture, and a Ct-W-Cr rotation compared with Ct-Ct are suggested to provide early indications of soil quality improvements attributed to reduced tillage, higher residue crops, and elimination of fallow periods for this semiarid region, which are practices that farmers can consider if their CRP land is returned to production. This study demonstrated that measures of the soil microbial community size, structure, and activities should be considered within the evaluation of changes in soil quality as affected by alternative management for continuous monoculture of cotton.
ACKNOWLEDGMENTS We would like to give special thanks to the 26 farmers participating in this study, who have allowed soil research on their farms. In addition, thanks to Mr. Jon Cotton and Mrs. Halee Hughes for their technical assistance and supervision of the project. SSSAJ: Volume 74: Number 4 • July–August 2010
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SSSAJ: Volume 74: Number 4 • July–August 2010
