Soil Nutrient Depletion Is Associated with the Presence of Burkholderia pseudomallei

Abstract

Burkholderia pseudomallei is a soil-dwelling bacterium and the cause of melioidosis, which kills an estimated 89,000 people per year worldwide. Agricultural workers are at high risk of infection due to repeated exposure to the bacterium. Little is known about the soil physicochemical properties associated with the presence or absence of the organism. Here, we evaluated the soil physicochemical properties and presence of B. pseudomallei in 6,100 soil samples collected from 61 rice fields in Thailand. The presence of B. pseudomallei was negatively associated with the proportion of clay, proportion of moisture, level of salinity, percentage of organic matter, presence of cadmium, and nutrient levels (phosphorus, potassium, calcium, magnesium, and iron). The presence of B. pseudomallei was not associated with the level of soil acidity (P = 0.54). In a multivariable logistic regression model, the presence of B. pseudomallei was negatively associated with the percentage of organic matter (odds ratio [OR], 0.06; 95% confidence interval [CI], 0.01 to 0.47; P = 0.007), level of salinity (OR, 0.06; 95% CI, 0.01 to 0.74; P = 0.03), and percentage of soil moisture (OR, 0.81; 95% CI, 0.66 to 1.00; P = 0.05). Our study suggests that B. pseudomallei thrives in rice fields that are nutrient depleted. Some agricultural practices result in a decline in soil nutrients, which may impact the presence and amount of B. pseudomallei bacteria in affected areas.IMPORTANCE Burkholderia pseudomallei is an environmental Gram-negative bacillus and the cause of melioidosis. Humans acquire the disease following skin inoculation, inhalation, or ingestion of the bacterium in the environment. The presence of B. pseudomallei in soil defines geographic regions where humans and livestock are at risk of melioidosis, yet little is known about the soil properties associated with the presence of the organism. We evaluated the soil properties and presence of B. pseudomallei in 61 rice fields in East, Central, and Northeast Thailand. We demonstrated that the organism was more commonly found in soils with lower levels of organic matter and nutrients, including phosphorus, potassium, calcium, magnesium, and iron. We also demonstrated that crop residue burning after harvest, which can reduce soil nutrients, was not uncommon. Some agricultural practices result in a decline in soil nutrients, which may impact the presence and amount of B. pseudomallei bacteria in affected areas.

Burkholderia pseudomallei in a lowland rice paddy: seasonal changes and influence of soil depth and physico-chemical properties

“…reported that a higher soil pH 6.05, a low water holding capacity, and low iron were associated with the presence of B. pseudomallei in soil from paddy fields in north east Thailand in the rainy season, whereas a high concentration of manganese correlated with the presence of the organism in the dry season 20 . More recently, workers in both Thailand and Australia have reported an association between sandy, nutrient-depleted soil and the presence of B. pseudomallei 14, 15 , contrasting with earlier reports of an association with soils enriched with organic matter from animal waste 12 .…”

“…also found B. pseudomallei to be negatively associated with soil organic matter content, concluding that B. pseudomallei may thrive in nutrient-depleted soils 15 . The data regarding iron are conflicting – the organism has been associated with both low 14, 15, 20 and high 9, 16, 17 levels of iron in natural environments, whilst iron enhanced the growth of B. pseudomallei in soil microcosms under laboratory conditions 35, 41 . B. pseudomallei is known to produce a siderophore and has other mechanisms that enable it to acquire iron.…”

Melioidosis: A Neglected Cause of Community-Acquired Pneumonia

“…9 Despite limited clinical reports, isolation of B. pseudomallei from soil and animals in Africa confirms hypotheses that melioidosis is widely distributed across the region. 10 Additionally, a novelty of B. pseudomallei is its ability to survive in extreme conditions, such as distilled water (for >16 years), 11 nutrient-depleted soil, 12 or desert environments. 10,13 Rivers may also be carriers and potential sentinels for B. pseudomallei, showing a shift in presence from 9% during the dry season to 57% in the rainy season (mainly in turbid water).…”

Melioidosis in the Torres Strait Islands, Australia: Exquisite Interplay between Pathogen, Host, and Environment

“…7 However, other studies have found a positive association with the proportion of sand. 8 Conversely, increasing soil salinity limits the bacterium's growth. 8 There are fewer data that define the effect of vegetation; however, the organism appears to thrive in rice fields and in the presence of grasses of the Aristida species.…”

“…8 Conversely, increasing soil salinity limits the bacterium's growth. 8 There are fewer data that define the effect of vegetation; however, the organism appears to thrive in rice fields and in the presence of grasses of the Aristida species. 9,10 The Torres Strait archipelago in tropical northern Australia covers an area of 48,000 km 2 .…”