Intra‐Aggregate Pore Structures and Escherichia coli Distribution by Water Flow within and Movement Out of Soil Macroaggregates

Soil aggregates are an important structural component of the soil matrix that could harbor Escherichia coli and provide an environment for its survival and water flow reentering. Knowledge of the exact pore locations within soil aggregates obtained using X-ray computed microtomography opens new opportunities for understanding microorganism movement within the soil matrix. The first objective of this study was to assess E. coli spatial distribution within soil macroaggregates and its potential for leaving the aggregates with the saturated water flow. The second objective was to study the relationships between the distribution and movement of E. coli within soil aggregates and the aggregates’ internal pore structures. We studied aggregates from the top (A) horizon of conventionally tilled (CT) and no-till (NT) corn–soybean–wheat rotations and native succession vegetation (NS) treatments at NSF Long-Term Ecological Research site, southwest Michigan. The results confirmed that E. coli movement in soil aggregates was mainly driven by water flow via capillary forces. E. coli r edistribution was most pronounced in CT aggregates, followed by NT, and was almost negligible in NS aggregates. Pore characteristics that positively contributed to E. coli redistribution through the aggregates were the maximum flow in the aggregate centers and the ratio of the maximum flow and pore tortuosity. The E. coli retention in the aggregate’s centers was positively related to porosity, percent of medium and large pores, and pore tortuosity.

[1]  V. O’Flaherty,et al.  Long-Term Persistence and Leaching of Escherichia coli in Temperate Maritime Soils , 2009, Applied and Environmental Microbiology.

[2]  J. Rose,et al.  Escherichia coli, enterococci, and Bacteroides thetaiotaomicron qPCR signals through wastewater and septage treatment. , 2011, Water research.

[3]  J. Zhuang,et al.  Virus retention and transport as influenced by different forms of soil organic matter. , 2003, Journal of environmental quality.

[4]  L. M. McDowell-Boyer,et al.  Particle transport through porous media , 1986 .

[5]  D. Tanaka,et al.  Soil Property Changes during Conversion from Perennial Vegetation to Annual Cropping , 2001 .

[6]  S. Mooney,et al.  Investigating the effects of organic and conventional management on soil aggregate stability using X‐ray computed tomography , 2009 .

[7]  W. B. Lindquist,et al.  Pore and throat size distributions measured from synchrotron X-ray tomographic images of Fontaineble , 2000 .

[8]  K. Ritz,et al.  Investigating microbial micro-habitat structure using X-ray computed tomography , 2006 .

[9]  C. Gerba Applied and theoretical aspects of virus adsorption to surfaces. , 1984, Advances in applied microbiology.

[10]  Rainer Horn,et al.  Three-dimensional quantification of intra-aggregate pore-space features using synchrotron-radiation-based microtomography , 2008 .

[11]  Y. Pachepsky,et al.  Effect of manure on Escherichia coli attachment to soil. , 2005, Journal of environmental quality.

[12]  J. Gaudet,et al.  Modification of Spatial Distribution of 2,4-Dichlorophenoxyacetic Acid Degrader Microhabitats during Growth in Soil Columns , 2004, Applied and Environmental Microbiology.

[13]  R. E. Sjogren Prolonged survival of an environmental Escherchia coli in laboratory soil microcosms , 1994 .

[14]  G. W. Thomas,et al.  Transport of Escherichia coli through intact and disturbed soil columns , 1985 .

[15]  J. Šimůnek,et al.  Transport and straining of E. coli O157:H7 in saturated porous media , 2006 .

[16]  R. Ketcham,et al.  Acquisition, optimization and interpretation of X-ray computed tomographic imagery: applications to the geosciences , 2001 .

[17]  G. Grundmann,et al.  Impact of the Microscale Distribution of a Pseudomonas Strain Introduced into Soil on Potential Contacts with Indigenous Bacteria , 2005, Applied and Environmental Microbiology.

[18]  L. Ruamps,et al.  Microbial biogeography at the soil pore scale , 2011 .

[19]  Roel Merckx,et al.  Spatial location of carbon decomposition in the soil pore system , 2004 .

[20]  André Revil,et al.  Permeability of shaly sands , 1999 .

[21]  G. Recorbet,et al.  Distribution of a genetically‐engineered Escherichia coli population introduced into soil , 1995, Letters in applied microbiology.

[22]  R. Vogt,et al.  Escherichia Coli O157:H7 Outbreak Associated with Consumption of Ground Beef, June–July 2002 , 2005, Public health reports.

[23]  Ana M. Tarquis,et al.  Multifractal analysis of the pore- and solid-phases in binary two-dimensional images of natural porous structures , 2006 .

[24]  Henry Lin,et al.  A comparison of fractal analytical methods on 2- and 3-dimensional computed tomographic scans of soil aggregates , 2006 .

[25]  F. Hellweger,et al.  Investigating the Fate and Transport of Escherichia coli in the Charles River, Boston, Using High‐Resolution Observation and Modeling 1 , 2008 .

[26]  J. A. Veen,et al.  Habitable pore space and survival ofRhizobium leguminosarum biovartrifolii introduced into soil , 1990, Microbial Ecology.

[27]  E. Perfect,et al.  Fecal coliform transport through intact soil blocks amended with poultry manure , 1998 .

[28]  Peter J. Eng,et al.  Geoscience applications of x-ray computed microtomography , 1999, Optics & Photonics.

[29]  K. Killham,et al.  Effect of substrate location in soil and soil pore-water regime on carbon turnover , 1993 .

[30]  R. Jamieson,et al.  Movement and persistence of fecal bacteria in agricultural soils and subsurface drainage water: A review , 2002 .

[31]  S. Yates,et al.  Straining of colloids at textural interfaces , 2005 .

[32]  R. Lal,et al.  Soil carbon dynamics in cropland and rangeland. , 2002, Environmental pollution.

[33]  Anthony R. Dexter,et al.  Advances in characterization of soil structure , 1988 .

[34]  H. E. Garrett,et al.  Influence of prairie restoration on CT-measured soil pore characteristics. , 2008, Journal of environmental quality.

[35]  Mark L. Rivers,et al.  Long‐term Differences in Tillage and Land Use Affect Intra‐aggregate Pore Heterogeneity , 2011 .

[36]  Richard A Haugland,et al.  Comparison of Enterococcus measurements in freshwater at two recreational beaches by quantitative polymerase chain reaction and membrane filter culture analysis. , 2005, Water research.

[37]  A. Kravchenko,et al.  Intra-aggregate Pore Characteristics: X-ray Computed Microtomography Analysis , 2012 .

[38]  K. Killham,et al.  Soil macropores and compaction control the leaching potential of Escherichia coli O157:H7. , 2005, Environmental microbiology.

[39]  A. Ibekwe,et al.  Detection and quantification of Escherichia coli O157:H7 in environmental samples by real-time PCR. , 2003, Journal of applied microbiology.

[40]  E. Topp,et al.  Development of a rapid quantitative PCR assay for direct detection and quantification of culturable and non-culturable Escherichia coli from agriculture watersheds. , 2007, Journal of microbiological methods.

[41]  C. Gerba,et al.  Effects of organic matter on virus transport in unsaturated flow , 1991, Applied and environmental microbiology.

[42]  S. Bradford,et al.  Straining, attachment, and detachment of cryptosporidium oocysts in saturated porous media. , 2005, Journal of environmental quality.

[43]  William P. Johnson,et al.  Role of hydrodynamic drag on microsphere deposition and re-entrainment in porous media under unfavorable conditions. , 2005, Environmental science & technology.

[44]  C. Gerba,et al.  MS-2 AND POLIOVIRUS TRANSPORT IN POROUS MEDIA : HYDROPHOBIC EFFECTS AND CHEMICAL PERTURBATIONS , 1993 .

[45]  J. Šimůnek,et al.  Straining and Attachment of Colloids in Physically Heterogeneous Porous Media , 2004 .

[46]  J. Schijven,et al.  Determining straining of Escherichia coli from breakthrough curves. , 2005, Journal of contaminant hydrology.

[47]  J. Rose,et al.  Relationships between intra-aggregate pore structures and distributions of Escherichia coli within soil macro-aggregates , 2013 .

[48]  S. Yates,et al.  Modeling colloid attachment, straining, and exclusion in saturated porous media. , 2003, Environmental science & technology.

[49]  G. Robertson,et al.  Land-Use Intensity Effects on Soil Organic Carbon Accumulation Rates and Mechanisms , 2007, Ecosystems.

[50]  N. Holden,et al.  Evaluating E. coli Transport Risk in Soil using Dye and Bromide Tracers , 2012 .

[51]  K. Paustian,et al.  Soil organic carbon pool changes following land‐use conversions , 2004 .

[52]  David L. Jones,et al.  Escherichia coli O157 survival following the surface and sub-surface application of human pathogen contaminated organic waste to soil , 2004 .

[53]  T. Vogel,et al.  A novel method for characterizing the microscale 3D spatial distribution of bacteria in soil , 2003 .

[54]  Yakov A. Pachepsky,et al.  Transport and fate of manure-borne pathogens: Modeling perspective , 2006 .

[55]  J. Six,et al.  A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics , 2004 .

[56]  Mark L. Rivers,et al.  Comparison of image segmentation methods in simulated 2D and 3D microtomographic images of soil aggregates , 2011 .

[57]  D. R. Fulkerson,et al.  Flows in Networks. , 1964 .

[58]  M. Goss,et al.  Movement of Faecal Bacteria through the Vadose Zone , 2003 .

[59]  Y. Pachepsky,et al.  Association of Fecal Coliforms With Soil Aggregates: Effect of Water Content and Bovine Manure Application , 2009 .

[60]  James J. Smith,et al.  Leaching of bacterial indicators of faecal contamination through four New Zealand soils , 2001 .

[61]  Andrey K. Guber,et al.  Transport and Retention of Manure‐Borne Coliforms in Soil , 2005 .

[62]  S. Dorevitch,et al.  Comparative Evaluation of Molecular and Culture Methods for Fecal Indicator Bacteria for Use in Inland Recreational Waters , 2011 .

[63]  Desmond F. Lawler,et al.  Depth filtration : Fundamental investigation through three-dimensional trajectory analysis , 1998 .

[64]  S. Yates,et al.  Significance of straining in colloid deposition: Evidence and implications , 2006 .

[65]  Richard M. Karp,et al.  Theoretical Improvements in Algorithmic Efficiency for Network Flow Problems , 1972, Combinatorial Optimization.

[66]  Claire Chenu,et al.  Short-term changes in the spatial distribution of microorganisms in soil aggregates as affected by glucose addition , 2001, Biology and Fertility of Soils.