A glimpse of Escherichia coli O157:H7 survival in soils from eastern China

https://doi.org/10.1016/j.scitotenv.2014.01.004Get rights and content

Highlights

  • E. coli O157:H7 survival times (td) varied in soils from eastern China.

  • Longer td values exist in soils from north-eastern than those from south-eastern China.

  • Soil MBC, Chloroflexi, TN and amorphous Al2O3 are important in affecting the td values.

  • Results provide information to reduce the potential risks of pathogen contamination.

Abstract

Escherichia coli O157:H7 (E. coli O157:H7) is an important food-borne pathogen, which continues to be a major public health concern worldwide. It is known that E. coli O157:H7 survive in soil environment might result in the contamination of fresh produce or water source. To investigate how the soils and their properties affect E. coli O157:H7 survival, we studied E. coli O157:H7 survival dynamics in 14 soils collected in eastern China from the warm-temperate zone to subtropical zone. Results showed that E. coli O157:H7 survival as a function of time can be well described by the Weibull model. The calculated td values (survival time to reach the detection limit, 100 colony forming units per gram oven-dried weight of soil) for the test soils were between 1.4 and 25.8 days. A significantly longer survival time (td) was observed in neutral or alkaline soils from north-eastern China (the warm-temperate zone) than that in acidic soils from south-eastern China (the subtropical zone). Distinct E. coli O157:H7 survival dynamics was related to soil properties. Stepwise multiple regression analysis revealed that the td values were significantly enhanced by soil microbial biomass carbon and total nitrogen, but were significantly reduced by amorphous Al2O3 and relative abundance of Chloroflexi. It should pay more attention to E. coli O157:H7 long survival in soils and its potential environmental contamination risk.

Introduction

Escherichia coli O157:H7 (E. coli O157:H7) is a food-borne pathogen that can cause watery diarrhea, hemorrhagic colitis, hemorrhagic uremic syndrome, and thrombotic thrombocytopenic purpura (Mead et al., 1999). The minimal infectious dose of E. coli O157:H7 for human is as few as 10 cells (Griffin and Tauxe, 1991). The first outbreak of E. coli O157:H7 infections caused by contaminated ground beef was reported in the USA in 1982 (Riley et al., 1983). Since then, many outbreaks and numerous sporadic cases of E. coli O157:H7 have been reported from all over the world, with several hundred severe outbreaks worldwide at mortality rate as high as 5–10% (Hedden, 2008). In the years from 1986 to 1988, E. coli O157:H7 strains in China were isolated from patients with diarrhea in Xuzhou City, Jiangsu Province (Xu et al., 1990). Later, during 1999–2000, several outbreaks in the middle-eastern areas of China, including Jiangsu, and the neighboring provinces of Anhui and Henan were reported (Ma et al., 2009). In recent years, extensive data from the epidemiologic survey disclosed that the presence of E. coli O157:H7 in external environments, such as excrements, sewages, foods, and soils for growing vegetables has been widely documented in China and other countries of the world (Banatvala et al., 2001, Islam et al., 2004, Ding et al., 2009, Ma et al., 2009, Brennan et al., 2010, Bradford et al., 2013).

More significantly, the carriage of E. coli O157:H7 would most likely result in the contamination of the environment. Studies reported that the manure-borne zoonotic pathogens (i.e., E. coli O157:H7, Salmonella spp., Listeria monocytogenes, et al.) can invade into the soil through sewage irrigation, runoff from stored manure, manure application or other processes (Solomon et al., 2002, van Elsas et al., 2011, Bradford et al., 2013). Furthermore, E. coli O157:H7 can survive in soil or soil-related (manure) environment for days to more than 1 year (Vidovic et al., 2007, Franz et al., 2008, Patel et al., 2010, Ma et al., 2011, Wang et al., 2013, Yao et al., 2013, Zhang et al., 2013), and it will be potentially transported to surface runoff, leached into groundwater, attached to plants, grew on plants surface, or even became internalized within plant tissue (Solomon et al., 2002, Islam et al., 2004, Brennan et al., 2010, Patel et al., 2010). Hence, a better understanding of the nature of E. coli O157:H7 survival in soil or soil-related (manure) environment will help in reducing its potential environmental contamination risk.

Previous studies observed that E. coli O157:H7 survival in soils were related to multiple factors, such as soil abiotic (nutrients, pH, moisture, temperature, texture, etc.), biotic parameters (indigenous microbial communities), and management practices (Islam et al., 2004, Vidovic et al., 2007, Franz et al., 2008, Patel et al., 2010, Ma et al., 2011, Ma et al., 2013, Wang et al., 2013, Yao et al., 2013, Zhang et al., 2013). For instances, Vidovic et al. (2007) revealed that the nutrient rich soils, in combination with moisture, might significantly extend E. coli O157:H7 survival in soil environment. Our recent findings showed that soil pH, organic carbon, and microbial community structure (represented as the ratio of bacteria phospholipid fatty acids (PLFAs) to fungi PLFAs) are the important factors in controlling E. coli O157:H7 survival in soils from vegetable fields (Yao et al., 2013). We also observed that E. coli O157:H7 can survive longer in soils under plastic-greenhouse cultivation than that in the corresponding open-field soils (Yao et al., 2013). A longer survival time of E. coli O157:H7 in soils implies that there is a high potential infection risk from the pathogen contaminated soils. Likewise, pathogen die-off rates are more critical to develop manure management recommendations. Consequently, the knowledge of E. coli O157:H7 survival in soils with different physical, chemical, and biological properties is critical to understand its fate in the environment to minimize the human infection from the pathogen.

The previous study reported that the survival kinetics of E. coli O157:H7 EDL933 (ATCC 43895) and its four mutant derivatives in the same soil were similar (Ma et al., 2011). Therefore, this study selected E. coli O157:H7 EDL933 (ATCC 43895) as a representative strain to investigate its survival in the 14 test soils from different climate zones from north to south in eastern China. The specific aims and significances of this study were to (1) determine the dynamics of E. coli O157:H7 survival in 14 soil samples collected from 12 different provinces in eastern China, (2) investigate the relationships between E. coli O157:H7 survival time and soil physicochemical and biological properties, and (3) provide information to understand the potential risks of pathogen contamination from soil and to protect human and environmental health.

Section snippets

Soils

The 14 soil samples (S1–S14) were collected from north (47.4°N, denoted as north-eastern China) to south (20.0°N, denoted as south-eastern China) in eastern China. Six soils (S1–S6) were from the warm-temperate zone in north-eastern China, while eight soils (S7–S14) were from the subtropical zone in south-eastern China. Specifically, soil S7 was from near the boundary between warm-temperate zone and subtropical zone, and its microbial community structure was found to be similar to the soil

Survival dynamics of E. coli O157:H7 in soils

No E. coli O157:H7 was detected neither by the plating analysis during the entire incubation period nor by the enrichment technique and multiplex PCR assay at 63 DAT in all inoculated and uninoculated soil samples. As shown in Fig. 2, the inoculated E. coli O157:H7 colonies recovered from the soils generally decreased with time over the 36-days incubation period. However, E. coli O157:H7 survival dynamics varied among the 14 test soils. E. coli O157:H7 declined rapidly in the five soils from

Discussion

As a general observation, the survival of E. coli O157:H7 showed a progressive decline in the 14 test soils with the incubation time. However, the dynamics of E. coli O157:H7 survival differed among the soils under the same temperature and moisture conditions. There existed a lag period at the beginning of inoculation (0–1 DAT) before E. coli O157:H7 declined with time in the soils S1–S6 from north-eastern China, while E. coli O157:H7 declined rapidly once the cells inoculated into the soils

Conclusions

Results from this study showed that E. coli O157:H7 survival varied in soils from eastern China. The E. coli O157:H7 could survive significantly longer in the north-eastern China soils than that in the south-eastern China soils under the experimental temperature (21 ± 1 °C) and moisture conditions (40% WHC). Soil microbial biomass carbon, Chloroflexi, TN and amorphous Al2O3 were the most important factors impacting E. coli O157:H7 survival time (td) in the test soils. It is difficult to control

Acknowledgments

This work was financially supported by the Major Program of National Natural Science Foundation of China (41130532) and the National Natural Science Foundation of China (40971255).

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    Present address: Jincai Ma, Biosciences and Biotechnology Division, Lawrence Livermore, National Laboratory, Livermore, CA 94550, USA.

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