Skip to main content
Log in

Impact of untreated urban waste on the prevalence and antibiotic resistance profiles of human opportunistic pathogens in agricultural soils from Burkina Faso

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

This study examined the long-term effects of the landfill disposal of untreated urban waste for soil fertilization on the prevalence and antibiotic resistance profiles of various human opportunistic pathogens in soils from Burkina Faso. Samples were collected at three sites in the periphery of Ouagadougou during two campaigns in 2008 and 2011. At each site, amendment led to changes in physico-chemical characteristics as shown by the increase in pH, CEC, total C, total N, and metal contents. Similarly, the numbers of total heterotrophic bacteria were higher in the amended fields than in the control ones. No sanitation indicators, i.e., coliforms, Staphylococci, and Enterococci, were detected. Pseudomonas aeruginosa and Burkholderia cepacia complex (Bcc) were detected at a low level in one amended field. Stenotrophomonas maltophilia was detected from both campaigns at the three sites in the amended fields and only once in an unamended field. Diversity analysis showed some opportunistic pathogen isolates to be closely related to reference clinical strains responsible for nosocomial- or community-acquired infections in Northern countries. Antibiotic resistance tests showed that P. aeruginosa and Bcc isolates had a wild-type phenotype and that most S. maltophilia isolates had a multi-drug resistance profile with resistance to 7 to 15 antibiotics. Then we were able to show that amendment led to an increase of some human opportunistic pathogens including multi-drug resistant isolates. Although the application of untreated urban waste increases both soil organic matter content and therefore soil fertility, the consequences of this practice on human health should be considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adamek M, Overhage J, Bathe S, Winter J, Fischer R, Schwartz T (2011) Genotyping of environmental and clinical Stenotrophomonas maltophilia isolates and their pathogenic potential. PLoS One 6:e27615. doi:10.1371/journal.pone.0027615

    Article  CAS  Google Scholar 

  • Afon A (2007) An analysis of solid waste generation in a traditional African city: the example of Ogbomoso, Nigeria. Environ Urban 19:527–537

    Article  Google Scholar 

  • Albiach R, Canet R, Pomares F, Ingelmo F (2000) Microbial biomass content and enzymatic activities after the application of organic amendments to a horticultural soil. Bioresour Technol 75:43–48

    Article  CAS  Google Scholar 

  • Ali SW, Li R, Zhou WY, Sun JQ, Guo P, Ma JP, Li SP (2010) Isolation and characterization of an abamectin-degrading Burkholderia cepacia-like GB-01 strain. Biodegradation 21:441–452. doi:10.1007/s10532-009-9314-7

    Article  CAS  Google Scholar 

  • Alvarez-Ortega C, Wiegand I, Olivares J, Hancock RE, Martínez JL (2011) The intrinsic resistome of Pseudomonas aeruginosa to β-lactams. Virulence 2:144–146

    Article  Google Scholar 

  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182

    Article  CAS  Google Scholar 

  • Balandreau J, Viallard V, Cournoyer B, Coenye T, Laevens S, Vandamme P (2001) Burkholderia cepacia genomovar III is a common plant-associated bacterium. Appl Environ Microbiol 67:982–985

    Article  CAS  Google Scholar 

  • Baquero F, Martinez JL, Canton R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Microbiol 19:260–265. doi:10.1016/j.copbio.2008.05.006

    CAS  Google Scholar 

  • Bastida F, Kandeler E, Moreno JL, Ros M, García C, Hernández T (2008) Application of fresh and composted organic wastes modifies structure, size and activity of soil microbial community under semiarid climate. Appl Soil Ecol 40:318–329

    Article  Google Scholar 

  • Berg G, Roskot N, Smalla K (1999) Genotypic and phenotypic relationships between clinical and environmental isolates of Stenotrophomonas maltophilia. J Clin Microbiol 37:3594–3600

    CAS  Google Scholar 

  • Berg G, Eberl L, Hartmann A (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7:1673–1685

    Article  CAS  Google Scholar 

  • Canton R, Morosini MI (2011) Emergence and spread of antibiotic resistance following exposure to antibiotics. FEMS Microbiol Reviews 35:977–991. doi:10.1111/j.1574-6976.2011.00295.x

    Article  CAS  Google Scholar 

  • Coenye T, Mahenthiralingam E, Henry D, LiPuma JJ, Laevens S, Gillis M, Speert DP, Vandamme P (2001) Burkholderia ambifaria sp. nov., anovel member of the Burkholderia cepacia complex including biocontrol and cystic fibrosis-related isolates. Int J Syst Evol Microbiol 51:1481–1490

    Article  CAS  Google Scholar 

  • Colinon C, Deredjian A, Hien E, Brothier E, Bouziri L, Cournoyer B, Hartman A, Henry S, Jolivet C, Ranjard L, Nazaret S (2013) Detection and enumeration of Pseudomonas aeruginosa in soil and manure assessed by an ecfX qPCR assay. J Appl Microbiol 114:1734–1749. doi:10.1111/jam.12189

    Article  CAS  Google Scholar 

  • Crecchio C, Curci M, Mininni R, Ricciuti P, Ruggiero P (2001) Short-term effects of municipal solid waste compost amendments on soil carbon and nitrogen content, some enzyme activities and genetic diversity. Biol Fertil Soils 34:311–318

    Article  CAS  Google Scholar 

  • Dalmastri C, Baldwin A, Tabacchioni S, Bevivino A, Mahenthiralingam E, Chiarini L, Dowson C (2007) Investigating Burkholderia cepacia complex populations recovered from Italian maize rhizosphere by multilocus sequence typing. Environ Microbiol 9:1632–1639

    Article  CAS  Google Scholar 

  • Debosz K, Petersen SO, Kure LK, Ambus P (2002) Evaluating effects of sewage sludge and household compost on soil physical, chemical and microbiological properties. Appl Soil Ecol 19:237–248

    Article  Google Scholar 

  • Deportes I, Benoit-Guyod JL, Zmirou D, Bouvier MC (1998) Microbial disinfection capacity of municipal solid waste (MSW) composting. J Appl Microbiol 85:238–246

    Article  CAS  Google Scholar 

  • Deredjian A, Colinon C, Hien E, Brothier E, Youenou B, Cournoyer B, Dequiedt S, Hartmann A, Jolivet C, Houot S, Ranjard L, Saby NPA, Nazaret S (2014) Low occurrence of Pseudomonas aeruginosa in agricultural soils with and without organic amendment. Front Cell Inf Microbiol 4:53. doi:10.3389/fcimb.2014.00053

    Article  Google Scholar 

  • Deredjian A, Alliot N, Blanchard L, Brothier E, Anane M, Cambier P, Jolivet C, Khelil MN, Nazaret S, Saby N, Thioulouse J, Favre-Bonté S (2016) Occurrence of Stenotrophomonas maltophilia in agricultural soils and antibiotic resistance properties. Res Microbiol 167:313–324. doi:10.1016/j.resmic.2016.01.001

    Article  CAS  Google Scholar 

  • Eaton D, Hilhorst T (2003) Opportunities for managing solid waste flows in the peri-urban interface of Bamako and Ouagadougou. Environ Urban 15:53–63

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nuc Ac Res 32:1792–1797

    Article  CAS  Google Scholar 

  • Edrington TS, Fox WE, Callaway TR, Anderson RC, Hoffman DW, Nisbet DJ (2009) Pathogen prevalence and influence of composted dairy manure application on antimicrobial resistance profiles of commensal soil bacteria. Foodborne Pathog Dis 6:217–224. doi:10.1089/fpd.2008.0184

    Article  CAS  Google Scholar 

  • FAO-IUSS-ISRIC (2006) World reference base for soil resources. A framework for international classification, correlation and communication. World Soil Resources Reports 103, Rome, p. 128

    Google Scholar 

  • Farzan A, Friendship RM, Cook A, Pollari F (2010) Occurrence of Salmonella, Campylobacter, Yersinia enterocolitica, Escherichia coli O157 and Listeria monocytogenes in swine. Zoonoses Public Health 57:388–396. doi:10.1111/j.18632378.2009.01248

    Article  CAS  Google Scholar 

  • Garbeva P, van Overbeek LS, van Vuurde JWL, van Elsas JD (2001) Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb Ecol 41:369–383

    Article  CAS  Google Scholar 

  • Garrec N, Picard-Bonnaud F, Pourcher AM (2003) Occurrence of Listeria sp and L. monocytogenes in sewage sludge used for land application: effect of dewatering, liming and storage in tank on survival of Listeria species. FEMS Immunol Med Microbiol 35:275–283

    Article  CAS  Google Scholar 

  • Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. doi:10.1093/molbev/msp259

    Article  CAS  Google Scholar 

  • Green SK, Schroth MN, Cho JJ, Kominos SK, Vitanza-Jack VB (1974) Agricultural plants and soil as a reservoir for Pseudomonas aeruginosa. Appl Microbiol 28:987–991

    CAS  Google Scholar 

  • Hagedorn C, Gould WD, Bardinelli TR, Gustavson DR (1987) A selective medium for enumeration and recovery of Pseudomonas cepacia biotypes from soil. Appl Environ Microbiol 53:2265–2268

    CAS  Google Scholar 

  • Hardoim PR, Hardoim CC, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7:e30438. doi:10.1371/journal.pone.0030438

    Article  CAS  Google Scholar 

  • Hassen A, Belguith K, Jedidi N, Cherif A, Cherif M, Boudabous A (2001) Microbial characterization during composting of municipal solid waste. Bioresour Technol 80:217–225

    Article  CAS  Google Scholar 

  • Henry DA, Campbell ME, Lipuma JJ, Speert DP (1997) Identification of Burkholderia cepacia isolates from patients with cystic fibrosis and use of a simple new selective medium. J Clin Microbiol 35:614–619

    CAS  Google Scholar 

  • Hickey WJ, Focht DD (1990) Degradation of mono-, di-, and trihalogenated benzoic acids by Pseudomonas aeruginosa JB2. Appl Environ Microbiol 56:3842–3850

    CAS  Google Scholar 

  • Holden MT, Seth-Smith HM, Crossman LC, Sebaihia M, Bentley SD, Cerdeño-Tárraga AM, Thomson NR, Bason N, Quail MA, Sharp S, Cherevach I, Churcher C, Goodhead I, Hauser H, Holroyd N, Mungall K, Scott P, Walker D, White B, Rose H, Iversen P, Mil-Homens D, Rocha EP, Fialho AM, Baldwin A, Dowson C, Barrell BG, Govan JR, Vandamme P, Hart CA, Mahenthiralingam E, Parkhill J (2009) The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191:261–277. doi:10.1128/JB.01230-08

    Article  CAS  Google Scholar 

  • Hu LF, Chang X, Ye Y, Wang ZX, Shao YB, Shi W, Li X, Li JB (2011) Stenotrophomonas maltophilia resistance to thrimethroprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 37:230–234. doi:10.1016/j.ijantimicag.2010.10.025

    Article  CAS  Google Scholar 

  • Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K (2014) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545. doi:10.1016/j.tim.2014.05.005

    Article  CAS  Google Scholar 

  • Kaboré TWT, Houot S, Hien E, Zombre P, Hien V, Masse D (2010) Effect of the raw materials and mixing ratio of composted wastes on the dynamic of organic matter stabilization and nitrogen availability in composts of sub-Saharan Africa. Bioresour Technol 101:1002–1013

    Article  Google Scholar 

  • Kaszab E, Szoboszlay S, Dobolyi C, Háhn J, Pék N, Kriszt B (2011) Antibiotic resistance profiles and virulence markers of Pseudomonas aeruginosa strains isolated from composts. Bioresour Technol 102:1543–1548. doi:10.1016/j.biortech.2010.08.027

    Article  CAS  Google Scholar 

  • Kuske CR, Barns SM, Grow CC, Merrill L, Dunbar J (2006) Environmental survey for four pathogenic bacteria and closely related species using phylogenetic and functional genes. J Forensic Sci 51:548–558

    Article  CAS  Google Scholar 

  • Lavenir R, Jocktane D, Laurent F, Nazaret S, Cournoyer B (2007) Improved reliability of Pseudomonas aeruginosa PCR detection by the use of the species-specific ecfX gene target. J Microbiol Methods 70:20–29

    Article  CAS  Google Scholar 

  • Lee DY, Lauder H, Cruwys H, Falletta P, Beaudette LA (2008) Development and application of an oligonucleotide microarray and real-time quantitative PCR for detection of wastewater bacterial pathogens. Sci Total Environ 398:203–211. doi:10.1016/j.scitotenv.2008.03.004

    Article  CAS  Google Scholar 

  • Livermore DM (2012) Fourteen years in resistance. Intern J Antimicrob Agents 39:283–294. doi:10.1016/j.ijantimicag.2011.12.012

    Article  CAS  Google Scholar 

  • Mahenthiralingam E, Bischof J, Byrne SK, Radomski C, Davies JE, Av-Gay VP (2000) DNA-based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis, Burkholderia multivorans, Burkholderia stabilis, and Burkholderia cepacia genomovars I and III. J Clin Microbiol 38:3165–3173

    CAS  Google Scholar 

  • Marecik R, Króliczak P, Czaczyk K, Białas W, Olejnik A, Cyplik P (2008) Atrazine degradation by aerobic microorganisms isolated from the rhizosphere of sweet flag (Acorus calamus L.). Biodegradation 19:293–301

    Article  CAS  Google Scholar 

  • Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663. doi:10.1111/1574-6976.12028

    Article  CAS  Google Scholar 

  • Meng J, Doyle MP (1997) Emerging issues in microbiological food safety. Annu Rev Nutr 17:255–275

    Article  CAS  Google Scholar 

  • Pinot C, Deredjian A, Nazaret S, Brothier E, Cournoyer B, Segonds C, Favre-Bonté S (2011) Identification of Stenotrophomonas maltophilia strains isolated from environmental and clinical samples: a rapid and efficient procedure. J Appl Microbiol 111:1185–1193. doi:10.1111/j.1365-2672.2011.05120

    Article  CAS  Google Scholar 

  • Pitcher DG, Saunders NA, Owen RJ (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8:151–156

    Article  CAS  Google Scholar 

  • Ramette A, LiPuma JJ, Tiedje JM (2005) Species abundance and diversity of Burkholderia cepacia complex in the environment. Appl Environ Microbiol 71:1193–1201

    Article  CAS  Google Scholar 

  • Sanchez MB, Hernandez A, Martinez JL (2009) Stenotrophomonas maltophilia drug resistance. Future Microbiol 4:655–660. doi:10.2217/fmb.09.45

    Article  CAS  Google Scholar 

  • Selezska K, Kazmierczak M, Müsken M, Garbe J, Schobert M, Häussler S, Wiehlmann L, Rohde C, Sikorski J (2012) Pseudomonas aeruginosa population structure revisited under environmental focus: impact of water quality and phage pressure. Environ Microbiol 14:1952–1967. doi:10.1111/j.1462-2920.2012.02719

    Article  CAS  Google Scholar 

  • Semenov AV, van Overbeek L, van Bruggen AH (2009) Percolation and survival of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in soil amended with contaminated dairy manure or slurry. Appl Environ Microbiol 75:3206–3215. doi:10.1128/AEM.01791-08

    Article  CAS  Google Scholar 

  • Singh RP, Singh P, Ibrahim MH, Hashim R (2011) Land application of sewage sludge: physicochemical and microbial response. Rev Environ Contam Toxicol 214:41–61. doi:10.1007/978-1-4614-0668-6

    CAS  Google Scholar 

  • Smith SR (2009) A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludge. Environ Int 35:142–156. doi:10.1016/j.envint.2008.06.009

    Article  CAS  Google Scholar 

  • Su JQ, Wei B, Ou-Yang WY, Huang FY, Zhao Y, HJ X, Zhu YG (2015) Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol 49:7356–7363. doi:10.1021/acs.est.5b01012

    Article  CAS  Google Scholar 

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

    Article  CAS  Google Scholar 

  • Trung TT, Hetzer A, Göhler A, Topfstedt E, Wuthiekanun V, Limmathurotsakul D, Peacock SJ, Steinmetz I (2011) Highly sensitive direct detection and quantification of Burkholderia pseudomallei bacteria in environmental soil samples by using real-time PCR. Appl Environ Microbiol 77:6486–6494. doi:10.1128/AEM.00735-11

    Article  CAS  Google Scholar 

  • Vedler E, Vahter M, Heinaru A (2004) The completely sequenced plasmid pEST4011 contains a novel IncP1 backbone and a catabolic transposon harboring tfd genes for 2,4-dichlorophenoxyacetic acid degradation. J Bacteriol 186:7161–7174

    Article  CAS  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    Article  CAS  Google Scholar 

  • Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 95:6578–6583

    Article  CAS  Google Scholar 

  • Yamamoto S, Harayama S (1998) Phylogenetic relationships of Pseudomonas putida strains deduced from the nucleotide sequences of gyrB, rpoD and 16S rRNA genes. Int J Syst Bacteriol 48:813–819

    Article  CAS  Google Scholar 

  • Youenou B, Brothier E, Nazaret S (2014) Diversity among strains of Pseudomonas aeruginosa from manure and soil, evaluated by multiple locus variable number tandem repeat analysis and antibiotic resistance profiles. Res Microbiol 165:2–13. doi:10.1016/j.resmic.2013.10.004

    Article  CAS  Google Scholar 

  • Youenou B, Favre-Bonté S, Bodilis J, Brothier E, Dubost A, Muller D, Nazaret S (2015) Comparative genomics of environmental and clinical Stenotrophomonas maltophilia strains with different antibiotic resistance profiles. Genome Biol Evol 7:2484–2505. doi:10.1093/gbe/evv161

    Article  CAS  Google Scholar 

  • Young JS, Gormley E, Wellington EM (2005) Molecular detection of Mycobacterium bovis and Mycobacterium bovis BCG (Pasteur) in soil. Appl Environ Microbiol 71:1946–1952

    Article  CAS  Google Scholar 

  • Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci U S A 110:3435–3440. doi:10.1073/pnas.1222743110

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a CORUS project of the French “Ministère des Affaires Etrangères”. B. Youenou was funded by a grant from the ADEME and the DGA. We thank the PARMIC technical platform and Rhône-Alpes Region Cluster “Environnement.”

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sylvie Nazaret.

Additional information

Responsible editor: Robert Duran

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Youenou, B., Hien, E., Deredjian, A. et al. Impact of untreated urban waste on the prevalence and antibiotic resistance profiles of human opportunistic pathogens in agricultural soils from Burkina Faso. Environ Sci Pollut Res 23, 25299–25311 (2016). https://doi.org/10.1007/s11356-016-7699-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7699-5

Keywords

Navigation