Enterobacteriaceae in Sewage Sludge and Digestate Intended for Soil Fertilization
Abstract
:1. Introduction
2. Materials and Methods
2.1. Determination of Bacteria Concentration Using Culture-Based Methods
2.1.1. Sample Collection
2.1.2. Microbiological Culture
2.2. Determination of Bacteria Species via Biochemical and Molecular Methods
2.2.1. Biochemical Tests
2.2.2. Molecular Tests
2.3. The Survival of E. coli Present in Organic Fertilizers on a Laboratory Scale
2.3.1. Samples
2.3.2. Inoculum Preparation
2.3.3. Main Experiment
2.3.4. Control Group
3. Results
3.1. Bacterial Concentration in Soil, Sewage Sludge and Digestate Samples
3.2. Species Diversity of Enterobacteriaceae Isolated from Soil, Sewage Sludge and Digestate
Enterobacteriaceae Isolated from Soil Samples (n = 82) | Sequence Result (Similarity with 16S rRNA) | Impact on Human Health | ||||
---|---|---|---|---|---|---|
Aeromonas spp. (n = 13) | A. hydrophila | 100% | MT572504.1 | opportunistic pathogen | emerging foodborne pathogen capable of causing human gastroenteritis | [19] |
A. sobria | 99.79% | OL778934.1 | food-borne illness, severe extraintestinal diseases: sepsis, peritonitis, meningitis | [20] | ||
A. media | 99.82% | CP038448.1 | food-borne illness, diarrhea | [21] | ||
A. veronii | 99.41% | KF853564.1 | gastroenteritis, bacteremia, septicemia, wound infections | [22] | ||
A. salmonicida | 99.54% | MT576565.1 | strain isolated from the blood of the patient with endocarditis | [23] | ||
A. encheleia | 100% | MT436428.1 | - | - | ||
Achromobacter spp. (n = 2) | A. xylosoxidans subsp. xylosoxidans | 99.77% | CP054571.1 | opportunistic pathogen | bacteremia, meningitis, urinary tract infection, endocarditis, pneumonia, especially in immunocompromised patients | [24] |
Buttiauxella spp. (n = 4) | B. agrestis | 99.57% | AP023184.1 | rare opportunistic pathogen | B. agrestis infection occurring at a post-cesarean surgical site | [25] |
B. gaviniae | 100% | MK905440.1 | - | clinical strain isolated from a urine sample from a spinal cord patient with urinary bladder pathology | [26] | |
Citrobacter spp. (n = 27) | C. braakii | 99.57% | MT534007.1 | rare pathogen, nosocomial infections | bacteremia in immunocompromised patients | [27,28] |
C. freundii | 100% | MH045703.1 | opportunistic pathogen of a wide spectrum of nosocomial infections | food poisoning, diarrhea, urinary tract infections | [29,30] | |
Enterobacter spp. (n = 37) | E. cloacae subsp. cloacae | 99.83% | MN181145.1 | opportunistic pathogen, nosocomial infections | lower respiratory tract infections, bacteremia | [31] |
E. ludwigii | 99.71% | MN826154.1 | unusual human pathogen | nosocomial bloodstream infection | [32] | |
E. asburiae | 99.67% | MN709316.1 | opportunistic pathogen | nosocomial infections | [33] | |
E. amnigenus biovar 1 | 100% | MN658356.1 | unusual human pathogen | nosocomial infections | [34] | |
Escherichia spp. (n = 14) | E. coli | 100% | MT192520.1 | opportunistic pathogen | enteritis, urinary tract infection, septicemia, neonatal meningitis, diarrhea | [35] |
E. vulneris | 99.57% | KX357823.1 | possible opportunistic pathogen | wound infections; complicated diarrhea and sepsis in an infant | [36,37] | |
Ewingella spp. (n = 1) | E. americana | 100% | MT998223.1 | rare opportunistic pathogen | bacteremia, pneumonia, conjunctivitis, Waterhouse–Friderichsen syndrome, peritonitis | [38] |
Gibbsiella spp. (n = 1) | G. quercinecans | 99.78% | MN822736.1 | - | - | - |
Hafnia spp. (n = 2) | H. alvei | 99.78% | CP050150.1 | potentially opportunistic pathogen | rare pneumonia cases | [39,40] |
Klebsiella spp. (12) | K. pneumoniae subsp. pneumoniae | 99.79% | OM017200.1 | opportunistic pathogen | urinary and respiratory tract infections, liver abscess, endophthalmitis, meningitis | [41] |
K. oxytoca | 100% | MT568561.1 | opportunistic pathogen | colitis, infective endocarditis, urinary and respiratory tract infections associated with nosocomial infections | [42] | |
Kluyvera spp. (n = 2) | K. intermedia | 99.78% | LT899978.1 | potential opportunistic pathogen | soft tissue infections, urinary tract infections, intra-abdominal abscesses, catheter-associated bloodstream infections, septic shock in immunocompromised patients (nosocomial infections) | [43] |
Pantoea spp. (n = 32) | P. agglomerans | 99.76% | MT635441.1 | opportunistic pathogen | septic arthritis, synovitis endophthalmitis, periostitis, endocarditis and osteomyelitis in the event of wound infection with plant material or as a hospital-acquired infection, mostly in immunocompromised individuals | [44] |
Pseudomonas spp. (n = 25) | P. tolaasii | 99.56% | MT561438.1 | - | - | - |
P. abietaniphila | 100% | MH379754.1 | - | - | - | |
P. fluroescens | 99.73% | OM827287.1 | scarce clinical significance | nosocomial infections | [45] | |
P. koreensis | 100% | MT501807.1 | - | possible nosocomial infections; a case of contact lens-related mixed infectious keratitis caused by A. fumigatus and P. koreensis | [46,47] | |
P. brassicacearum subsp. neoaurantiaca | 99.80 | MT634587.1 | - | - | - | |
P. chlororaphis | 100% | KJ530973.1 | - | - | - | |
P. kilonensis | 99.57% | MT102732.1 | - | - | - | |
Rahnella spp. (n = 18) | R. aquatilis | 99.77% | MN826573.1 | possible opportunistic pathogen | possible role as the pathogen responsible for ventilator-associated pneumonia associated with nosocomial infections in immunocompromised patients | [48] |
R. victoriana | 99.78% | OK658118.1 | - | - | - | |
Raoultella spp. (n = 5) | R. terrigena | 100% | MT545123.1 | opportunistic pathogen | cases of bloodstream, urinary tract, respiratory tract or bile tract infections mostly associated with nosocomial infections; subungual abscess caused by R. terrigena | [49,50] |
R. ornithinolytica | 100% | MT568560.1 | ||||
Serratia spp. (n = 44) | S. plymuthica | 99.58% | CP053398.1 | rare (unusual) human pathogen | associated with chronic osteomyelitis and cases of sepsis secondary to central venous catheter infection | [51] |
S. liquefaciens | 100% | MT279350.1 | opportunistic pathogen | cause of transfusion-related sepsis, meningitis thrombophlebitis, corneal ulcers | [52] | |
S. fonticola | 100% | MN227497.1 | rare (unusual) human pathogen | skin and soft tissue infections | [53,54] | |
S. quinivorans | 99.71% | MT256279.1 | - | - | - | |
S. proteamaculans | 100% | MK530287.1 | opportunistic pathogen | able to penetrate eukaryotic cells | [55] | |
S. marcescens | 99.85% | MT598027.1 | opportunistic pathogen | urinary tract infections, pneumonia, intravenous catheter-associated infections, osteomyelitis, endocarditis | [51,56] | |
S. entomophila | 99.83% | MK216954.1 | - | - | - | |
Yersinia spp. (n = 2) | Y. enterocolitica | 99.14% | MN905014.1 | zoonotic pathogen | enteric infections, mesenteric lymphadenitis, reactive arthritis, erythema nodosum | [57] |
Enterobacteriaceae Isolated from the Sewage Sludge and Digestate Samples (n = 18) | Sequence Result (Similarity with 16S rRNA) | Impact on Human Health | ||||
---|---|---|---|---|---|---|
Sewage Sludge Samples | Digestate Samples | |||||
Aeromonas salmonicida | 100% | MT576565.1 | 100% | KF551980.1 | As in Table 2 | |
Alcaligenes faecalis | 99.76% | MT277037.1 | - | - | sporadic cases of endocarditis, meningitis, chronic otitis, pyelonephritis, bacteremia, peritonitis, endophthalmitis, abscesses, often associated with nosocomial infections | [58] |
Comamonas jiangduensis | 99.80% | NR_109655.1 | - | - | - | - |
Citrobacter freundii | - | - | 100% | OM666544.1 | As in Table 2 | |
Citrobacter gillenii | - | - | 100% | MT436425.1 | the strains were isolated from human stool, urine and blood | [59] |
Enterobacter cloacae | 99.61% | MN006380.1 | - | - | As in Table 2 | |
Escherichia coli | 100% | OM982954.1 | 100% | CP091756.1 | As in Table 2 | |
Hafnia alvei | 99.39% | CP050150.1 | - | - | As in Table 2 | |
Ignatzschineria indica | 99.75% | LC010924.1 | rare cases of bacteremia mostly associated with wound myiasis | [60] | ||
Klebsiella oxytoca | 99.48% | MT509911.1 | - | - | As in Table 2 | |
Klebsiella pneumoniae | - | - | 99.79% | OM978275.1 | As in Table 2 | |
Morganella morganii subsp. morganii | 99.80% | CP043955.1 | - | - | opportunistic infections: urinary tract infection, wound infection, arthritis, prostatitis | [61] |
Proteus mirabilis | - | - | 99.63% | OM882519.1 | catheter-associated urinary tract infections | [62] |
Salmonella enterica subsp. enterica serovar Johannesburg | - | - | 100% | CP049308.1 | gastrointestinal infection—salmonellosis | [63] |
Yersinia enterocolitica | - | - | 99.71% | MK910030.1 | As in Table 2 | |
Yersinia frederiksenii | 100% | KC776774.1 | - | - | possible diarrheal diseases | [64] |
Yersinia intermedia | - | - | 99.82% | MN416246.1 | strains were isolated from human stool and urine samples and from wound infections but rarely associated with human diseases | [65] |
3.3. The Survival of E. coli in Soil Samples Fertilized with Sewage Sludge and Digestate in Laboratory Conditions
3.3.1. Main Experiment
3.3.2. Control Experiment
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Component | Total No. of Enterobacteriaceae [CFU/g] | Total No. of Escherichia coli [CFU/g] |
---|---|---|
Universal soil | 3.1 × 102 | <1 |
Clay soil | 26 | <1 |
Sewage sludge | 2.5 × 106 | 1.4 × 104 |
Digestate | 1.3 × 106 | 1.0 × 104 |
Type of Samples | Bacterial Concentration [CFU/g] | ||||||||
---|---|---|---|---|---|---|---|---|---|
Total Mesophilic Bacteria | Enterobacteriaceae | Escherichia coli | |||||||
Positive Samples | Median (Range) | Mean ± S.D. | Positive Samples | Median (Range) | Mean ± S.D. | Positive Samples | Median (Range) | Mean ± S.D. | |
Soil n = 82 | 82 (100%) | 3.8 × 105 (1.1 × 105−4.6 × 106) | 4.6 × 105 ± 5.1 × 105 | 82 (100%) | 6.3 × 102 (1.2 × 101−3.2 × 105) | 1.1 × 104 ± 4.3 × 104 | 2 (2.4%) | − | − |
Sewage sludge n = 9 | 8 (88.9%) | 3.7 × 107 (1.6 × 103−5.7 × 108) | 1.4 × 108 ± 2.1 × 108 | 6 (66.7%) | 7.2 × 105 (1.5 × 103−2.2 × 106) | 9.4 × 105 ± 9.9 × 105 | 4 (44.4%) | 1.2 × 104 (3.8 × 102−4.2 × 104) | 1.7 × 104 ± 2.0 × 104 |
Digestate n = 9 | 9 (100%) | 1.2 × 108 (1.0 × 107−9.8 × 108) | 2.6 × 108 ± 3.4 × 108 | 9 (100%) | 2.8 × 106 (3.1× 105−2.1 × 107) | 5.6 × 106 ± 7.3 × 106 | 6 (66.7%) | 3.1 × 104 (8.0 × 101−9.9 × 106) | 1.7 × 106 ± 4.0 × 106 |
Type of Sample: Non-Sterile Soil + Sterile Sewage Sludge/Digestate + E. coli Suspension | Week | Enterobacteriaceae [CFU/g] | E. coli [CFU/g] |
---|---|---|---|
universal soil + sewage sludge + E. coli (8.3 dm3 + 14.2 g + 1.8 mL) | 0 | 3.3 × 103 | 1.1 × 103 |
1 | 1.3 × 103 | 5.7 × 103 | |
2 | 1.8 × 102 | <1 | |
3 | 41 | <1 | |
universal soil + sewage sludge + E. coli (8.3 dm3 + 88.5 g + 11.1 mL) | 0 | 1.2 × 104 | 1.6 × 103 |
1 | 9.7 × 103 | 3.5 × 103 | |
2 | 8.0 × 102 | 2.4 × 103 | |
3 | 1.3 × 102 | <1 | |
universal soil + digestate + E. coli (8.3 dm3 + 14.2 g + 1.8 mL) | 0 | 1.4 × 103 | 0.9 × 102 |
1 | 3.2 × 103 | 1.0 × 102 | |
2 | 2.3 × 102 | <1 | |
3 | 67 | <1 | |
universal soil + digestate + E. coli (8.3 dm3 + 88.5 g + 11.1 mL) | 0 | 3.0 × 103 | 3.9 × 103 |
1 | 6.4 × 103 | 4.0 × 103 | |
2 | 1.8 × 102 | 1.0 × 102 | |
3 | 1.8 × 102 | <1 | |
clay soil + sewage sludge + E. coli (8.3 dm3 + 14.2 g + 1.8 mL) | 0 | 2.2 × 103 | 1.8 × 103 |
1 | 2.4 × 102 | 1.3 × 102 | |
2 | 1.2 × 102 | 21 | |
3 | 83 | <1 | |
clay soil + sewage sludge + E. coli (8.3 dm3 + 88.5 g + 11.1 mL) | 0 | 1.0 × 104 | 1.3 × 104 |
1 | 2.9 × 105 | 1.8 × 105 | |
2 | 1.6 × 104 | 5.3 × 103 | |
3 | 6.0 × 102 | 2.8 × 102 | |
clay soil + digestate + E. coli (8.3 dm3 + 14.2 g + 1.8 mL) | 0 | 1.8 × 103 | 3.1 × 103 |
1 | 1.9 × 102 | 1.6 × 102 | |
2 | 41 | 13 | |
3 | 15 | <1 | |
clay soil + digestate + E. coli (8.3 dm3 + 88.5 g + 11.1 mL) | 0 | 1.6 × 104 | 1.5 × 104 |
1 | 1.8 × 103 | 1.3 × 103 | |
2 | 2.1 × 102 | 25 | |
3 | 2.2 × 102 | 16 |
Type of Sample: Non-Sterile Soil + Non-Sterile Sewage Sludge/Digestate | Week | Enterobacteriaceae [CFU/g] | E. coli [CFU/g] |
---|---|---|---|
universal soil + sewage sludge (8.3 dm3 + 14.2 g) | 0 | 1.3 × 104 | <1 |
1 | 3.5 × 102 | <1 | |
2 | 1.2 × 102 | <1 | |
3 | 1.1 × 102 | <1 | |
universal soil + sewage sludge (8.3 dm3 + 88.5 g) | 0 | 3.5 × 103 | 2.5 × 102 |
1 | 9.5 × 102 | 65 | |
2 | 1.2 × 102 | <1 | |
3 | 1.7 × 102 | <1 | |
universal soil + digestate (8.3 dm3 + 14.2 g) | 0 | 2.3 × 103 | <1 |
1 | 3.3 × 102 | <1 | |
2 | 37 | <1 | |
3 | 84 | <1 | |
universal soil + digestate (8.3 dm3 + 88.5 g) | 0 | 1.3 × 103 | <1 |
1 | 4.6 × 102 | <1 | |
2 | 57 | <1 | |
3 | 97 | <1 | |
clay soil + sewage sludge (8.3 dm3 + 14.2 g) | 0 | 95 | <1 |
1 | 1.3 × 103 | <1 | |
2 | 2.8 × 102 | <1 | |
3 | 32 | <1 | |
clay soil + sewage sludge (8.3 dm3 + 88.5 g) | 0 | 117 | <1 |
1 | 9.3 × 103 | <1 | |
2 | 3.0 × 102 | <1 | |
3 | 55 | <1 | |
clay soil + digestate (8.3 dm3 + 14.2 g) | 0 | 49 | <1 |
1 | 1.1 × 102 | <1 | |
2 | 11 | <1 | |
3 | 15 | <1 | |
clay soil + digestate (8.3 dm3 + 88.5 g) | 0 | 1.3 × 102 | <1 |
1 | 1.5 × 103 | <1 | |
2 | 1.4 × 102 | <1 | |
3 | 1.8 × 102 | <1 |
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Wójcik-Fatla, A.; Farian, E.; Kowalczyk, K.; Sroka, J.; Skowron, P.; Siebielec, G.; Zdybel, J.M.; Jadczyszyn, T.; Cencek, T. Enterobacteriaceae in Sewage Sludge and Digestate Intended for Soil Fertilization. Pathogens 2024, 13, 1056. https://doi.org/10.3390/pathogens13121056
Wójcik-Fatla A, Farian E, Kowalczyk K, Sroka J, Skowron P, Siebielec G, Zdybel JM, Jadczyszyn T, Cencek T. Enterobacteriaceae in Sewage Sludge and Digestate Intended for Soil Fertilization. Pathogens. 2024; 13(12):1056. https://doi.org/10.3390/pathogens13121056
Chicago/Turabian StyleWójcik-Fatla, Angelina, Ewelina Farian, Katarzyna Kowalczyk, Jacek Sroka, Piotr Skowron, Grzegorz Siebielec, Jolanta Małgorzata Zdybel, Tamara Jadczyszyn, and Tomasz Cencek. 2024. "Enterobacteriaceae in Sewage Sludge and Digestate Intended for Soil Fertilization" Pathogens 13, no. 12: 1056. https://doi.org/10.3390/pathogens13121056
APA StyleWójcik-Fatla, A., Farian, E., Kowalczyk, K., Sroka, J., Skowron, P., Siebielec, G., Zdybel, J. M., Jadczyszyn, T., & Cencek, T. (2024). Enterobacteriaceae in Sewage Sludge and Digestate Intended for Soil Fertilization. Pathogens, 13(12), 1056. https://doi.org/10.3390/pathogens13121056