A review of the abundance, behaviour and detection of clostridial pathogens in agricultural soils

European Journal of Soil Science - Tập 70 Số 4 - Trang 911-929 - 2019
Joseph Samuel Palmer1,2, Rupert Hough2, Helen West1, Lisa M. Avery2
1Agricultural and Environmental Sciences, School of Biosciences, University of Nottingham, Loughborough, UK
2Environmental and Biochemical Sciences, The James Hutton Institute, Aberdeen, UK

Tóm tắt

AbstractThe soil is a reservoir for various clostridial pathogens, with agricultural soils representing a major source of contamination for overlying crops and grazing livestock. Understanding the prevalence and behaviour of pathogens in these soils is fundamental to ascertaining and mitigating the risk of disease from agroecosystems. This article reviews research pertaining to the overall distribution and abundance of clostridial pathogens in the soil while identifying possible environmental and soil factors influencing their behaviour. Large‐scale soil screens have identified pathogens across the globe, although some Clostridium botulinum toxinotypes are more prevalent in certain geographic regions. Faecal inputs and organic waste amendments to the soil can elevate the levels of enteric clostridial pathogens in the soil and the subsequent disease risk, as highlighted by case–control studies. The ability of Clostridia to sporulate results in their long‐term persistence post‐introduction, increasing the time period for disease transmission. Regularly or permanently saturated soils may also enhance survival, or potentially facilitate the regrowth of some indigenous or introduced Clostridia. This is supported by the high prevalence of Clostridia in paddy soils, greater detection of pathogens in flooded soils, and the higher onset of some clostridial diseases in regions with poorly drained soils. Future research should elucidate soil types and environmental conditions which can enhance pathogen survival/regrowth. The adoption of molecular and sequencing technologies for future diagnostics can facilitate more sensitive detection and a higher resolution of pathogen typing, allowing a better understanding of pathogen population dynamics in farm soils and disease epidemiology.Highlights Understanding the behaviour of soil‐borne clostridial pathogens is key for disease management. Soil, environmental and management factors affecting pathogen survival/introduction are discussed. Soil waterlogging and application of organic soil amendments may increase the number of soil pathogens. More pathogen surveillance and standardisation of diagnostics to better understand behaviour is needed.

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Tài liệu tham khảo

Abo‐Remela E., 2012, Effects of stressors on the expression of virulence factors and cell survival in Clostridium perfringens, Journal of the Kanazawa University Complete Medical Association, 121, 47

10.1016/j.soilbio.2008.07.022

10.7326/0003-4819-154-5-201103010-00007

10.1099/00222615-45-2-133

Albrecht J.A. (2005).Clostridium perfringens. University of Nebraska‐Food Safety. Institute of Agriculture and Natural Resources. Retrieved fromhttps://food.unl.edu/clostridium-perfringens.

10.1111/j.1365-2672.2010.04790.x

10.1016/j.watres.2005.03.016

10.3122/jabfm.2012.05.110226

10.2746/042516403775600505

10.1111/j.1439-0450.2000.00426.x

10.1128/JB.184.9.2333-2343.2002

10.1134/S0003683807060014

10.1016/j.agee.2011.05.021

10.1111/j.1365-2672.1982.tb01283.x

10.1007/s00203-004-0721-1

10.1016/S0168-1605(01)00680-8

10.1016/S0038-0717(98)00043-1

Burke C., 2014, Resolving microbial microdiversity with high accuracy full length 16S rRNA Illumina sequencing, Cold Spring Harbor Labs Journals.

Burlage R. S., 1985, Comparison of the PRAS II, AN‐Ident, and RapID‐ANA systems for identification of anaerobic bacteria, Journal of Clinical Microbiology, 22, 32, 10.1128/jcm.22.1.32-35.1985

Chessbrough M., 2002, District Laboratory Practice in Tropical Countries. Part 2

10.1111/j.1365-2389.2005.00688.x

10.1099/00207713-44-4-812

10.1002/1521-3803(20010401)45:2<125::AID-FOOD125>3.0.CO;2-8

10.1007/BF02091912

10.1016/j.mimet.2008.04.011

10.1016/S0958-1669(02)00314-2

10.1128/AEM.00805-09

10.1016/j.anaerobe.2005.04.006

10.1007/BF02816236

10.1371/journal.pone.0019993

Dodds K. L., 1992, Clostridium botulinum: Ecology and control in foods, 21

10.3390/d4040375

Dudley D. J., 1980, Enumeration of potentially pathogenic bacteria from sewage sludges, Applied and Environmental Microbiology, 39, 118, 10.1128/aem.39.1.118-126.1980

10.3389/fmicb.2014.00287

10.1046/j.1365-2672.1997.00225.x

10.1016/j.ijfoodmicro.2010.04.006

10.1111/j.1365-2672.2009.04215.x

10.1016/j.foodcont.2014.08.024

10.1016/j.ijfoodmicro.2011.02.001

10.1146/annurev.phyto.42.012604.135455

10.1016/S0043-1354(03)00394-4

10.1111/j.1574-6941.2006.00183.x

Ghoddusi H. B., 2013, Growth limiting pH, water activity, and temperature for neurotoxigenic strains of Clostridium butyricum, International Scholarly Research Notices, 2013

10.1016/j.femsec.2005.04.003

10.1128/AEM.71.2.1079-1083.2005

10.1128/JCM.01796-09

10.1016/j.anaerobe.2008.06.002

10.20506/rst.10.3.569

10.1016/S0147-9571(99)00078-8

10.1128/AEM.01849-13

10.1128/CMR.3.1.66

10.1016/j.micres.2005.12.002

Head C. B., 1988, Comparison of API ZYM system with API AN‐Ident, API 20A, Minitek Anaerobe II, and RapID‐ANA systems for identification of Clostridium difficile, Journal of Clinical Microbiology, 26, 144, 10.1128/jcm.26.1.144-146.1988

10.1016/j.watres.2005.10.030

10.1093/infdis/125.1.17

10.1111/j.1365-2958.2008.06192.x

10.1111/j.2042-3306.1999.tb03857.x

10.1128/aem.39.4.764-769.1980

10.1111/j.1574-6941.2002.tb00921.x

10.1111/j.1365-2958.2006.05028.x

10.1094/Phyto-67-651

Jamieson R. C., 2002, Movement and persistence of fecal bacteria in agricultural soils and subsurface drainage water: A review, Canadian Biosystems Engineering, 44, 1

10.1128/AEM.72.3.1719-1728.2006

10.1099/mic.0.27017-0

Jeffery S.&Van der Putten W.H.(2011).Soil borne human diseases. Retrieved from:https://www.kiza.beroepsziekten.nl/sites/default/files/documenten/soil borne human diseases jeffery putte 2011.pdf.

10.1111/j.1745-4565.1986.tb00557.x

10.1128/IAI.71.4.1784-1793.2003

10.1128/JCM.01275-06

Khoruts A., 2010, Changes in the composition of the human fecal microbiome following bacteriotherapy for recurrent Clostridium difficile‐associated diarrhea, Journal of Clinical Gastroenterology, 44, 354, 10.1097/MCG.0b013e3181c87e02

Kim J., 2004, Distribution and antimicrobial susceptibility of Clostridium species in soil contaminated with domestic livestock feces of Korea, Journal of Microbiology and Biotechnology, 14, 401

10.1016/j.mimet.2004.04.006

Knechtges P. L., 2011, Food safety: Theory and practice

10.1111/j.1556-4029.2006.00131.x

Kusliene G., 2010, The influence of land use on soil organic carbon and nitrogen content and redox potential, Zemdirbyste ‐ Agriculture

10.1016/j.solener.2010.01.023

10.1146/annurev.mi.49.100195.002151

10.1111/j.1574-6941.2001.tb00895.x

10.1016/j.cvfa.2010.10.009

10.1128/AEM.01075-07

10.1111/j.1574-6976.2000.tb00563.x

10.1016/j.fm.2010.03.020

10.1128/AEM.67.12.5694-5699.2001

10.1111/j.1574-695X.1999.tb01293.x

10.2136/sssaj1984.03615995004800040019x

10.1128/AEM.71.7.4137-4139.2005

10.1111/j.1750-3841.2008.00984.x

10.1111/j.1462-2920.2008.01572.x

10.1016/0929-1393(94)00039-A

10.2746/0425164044868594

10.1007/978-1-59745-501-5_3

10.1128/AEM.02275-12

10.1099/00222615-48-2-133

10.1016/j.geoderma.2015.08.042

10.1007/978-1-4757-9718-3

10.7883/yoken1952.28.201

10.1128/AEM.70.11.6580-6586.2004

10.1016/j.jenvman.2008.01.009

Moynihan E.L. (2012).Interactions between microbial community structure and pathogen survival in soil. Cranfield Bedford England: Cranfield University Cranfield Bedford UK. Retrieved fromhttps://dspace.lib.cranfield.ac.uk/handle/1826/7297.

10.1128/JB.02230-14

Natsch A., 1996, Importance of preferential flow and soil management in vertical transport of a biocontrol strain of Pseudomonas fluorescens in structured field soil, Applied and Environmental Microbiology, 62, 33, 10.1128/aem.62.1.33-40.1996

10.4067/S0718-58392015000300005

10.1016/j.ijfoodmicro.2010.01.021

10.2746/0425164044868639

10.1093/infdis/16.2.132

10.1016/S0065-2164(08)70152-7

10.1111/ejss.12216

10.1006/anae.2001.0373

10.1016/B978-012164730-8/50065-4

10.3390/toxins9010038

10.1080/10643380701664748

10.1111/j.1365-2672.1985.tb01463.x

10.1111/j.1469-0691.2008.02092.x

10.1309/AJCPTP5XKRSNXVIL

10.1016/S0966-842X(98)01430-9

10.1128/AEM.71.11.6998-7007.2005

10.1111/evj.12254

10.1016/j.toxicon.2013.05.003

10.1128/JB.01226-09

10.4315/0362-028X-66.8.1402

10.1128/AEM.03712-15

10.1038/ismej.2007.53

10.1016/j.soilbio.2012.05.021

10.1016/j.geoderma.2011.08.014

10.1016/j.biortech.2007.09.071

10.1128/JCM.03385-14

10.7589/0090-3558-29.4.533

10.7589/0090-3558-34.4.830

10.1016/S0378-1135(02)00002-0

10.1053/rvsc.2000.0431

10.4103/0255-0857.55443

10.1093/infdis/31.6.610

Schubert S.&Kostrzewa M.(2016).Future trends and perspectives of MALDI‐TOF MS in the microbiology laboratory. In M. Kostrzewa (Ed.) MALDI‐TOF mass spectrometry in microbiology(pp.157–160) Norfolk England: Caister Academic Press.

10.1128/JB.00787-10

10.1111/j.1348-0421.1977.tb00274.x

10.1016/j.tim.2007.02.004

10.1136/vr.101184

10.1016/j.trstmh.2006.01.009

10.1371/journal.pone.0107777

10.1016/j.mimet.2007.02.014

10.1017/S0022172400026024

10.1017/S0022172400024906

10.1017/S0022172400063300

Smith L. D., 1975, Common Mesophilic Anaerobes, Including Clostridium botulinum and Clostridium tetani, in 21 Soil Specimens, Applied and Environmental Microbiology, 29, 590, 10.1128/am.29.5.590-594.1975

Smith L. D., 1975, Inhibition of Clostridium botulinum by Strains of Clostridium perfringens Isolated from Soil, Applied and Environmental Microbiology, 30, 319, 10.1128/am.30.2.319-323.1975

Smith L. D., 1978, The occurrence of Clostridium botulinum and Clostridium tetani in the soil of the United States, Health Laboratory Science, 15, 74

10.1016/j.meegid.2014.12.002

10.1128/CMR.9.2.216

10.1016/j.vetmic.2009.07.003

Sonnabend W. F., 1987, Isolation of Clostridium botulinum type G from Swiss soil specimens by using sequential steps in an identification scheme, Applied and Environmental Microbiology, 53, 1880, 10.1128/aem.53.8.1880-1884.1987

10.1111/j.1574-695X.1999.tb01291.x

10.1007/s12223-013-0257-3

10.1186/1471-2164-14-333

10.1136/bmj.310.6991.1375

Tally F. P., 1975, Oxygen tolerance of fresh clinical anaerobic bacteria, Journal of Clinical Microbiology, 1, 161, 10.1128/jcm.1.2.161-164.1975

10.2166/wh.2005.0015

10.1016/S0140-6736(14)60236-1

10.1016/S0929-1393(99)00026-8

10.2460/javma.2002.220.342

Torniainen M., 2011, Animal hygiene and sustainable livestock production, 1103

10.1111/j.1574-6941.2006.00085.x

10.1007/BF00337375

10.1080/03079450400013162

10.1016/j.livsci.2006.03.017

10.1128/AEM.01191-13

10.1007/s10661-014-3807-5

10.1016/j.anaerobe.2011.05.004

10.1111/j.2042-3306.2010.00105.x

10.1128/AEM.67.3.1318-1327.2001

10.1128/AEM.01159-15

10.1111/j.1365-2672.2008.03965.x

10.1007/978-0-387-68489-5

WHO. (2016).WHO vaccine‐preventable diseases: monitoring system 2016 global summary. Retrieved from:http://apps.who.int/immunization_monitoring/globalsummary/timeseries/tsincidencettetanus.html.

Wilkins C., 1988, Occurrence of Clostridium tetani in soil and horses, South African Medical Journal, 73, 718

10.1111/j.1574-6976.1997.tb00351.x

10.7589/0090-3558-23.1.67

10.1016/j.prevetmed.2017.01.019

10.1016/S1090-0233(98)80055-5

10.1016/j.cveq.2009.04.006

10.1111/j.1348-0421.1988.tb01419.x

10.1128/AEM.01966-10