Effects of Bacterial-Feeding Nematodes and Glucose on Phenanthrene Removal by Pseudomonas putida

doi:10.1016/S1002-0160(15)60103-5

Pedosphere

Volume 27, Issue 1, February 2017, Pages 165-171

https://doi.org/10.1016/S1002-0160(15)60103-5 Get rights and content

Abstract

Bacterial–feeding nematodes can promote the bacterial activity through feeding. Bacterial abundance and their activity affect the degradation of polycyclic aromatic hydrocarbons (PAH) such as phenanthrene. The effects of bacterial–feeding nematodes, bacteria, and their interactions on the degradation of phenanthrene with or without glucose were studied through a microcosm experiment. The results showed that up to 57.0% of phenanthrene in mineral medium contaminated with phenanthrene was degraded in the control with bacteria alone and bacteria with the presence of nematodes and/or glucose increased the degradation of phenanthrene by 25.6% to 36.6%. Although both nematode and bacteria abundance decreased gradually, catechol 2,3–dioxygenase (C23O) activity increased during the incubation period. Compared with bacteria alone, the presence of nematodes significantly increased C23O activity as well as the abundance of bacteria; this effect was more pronounced when glucose was present. The results imply that nematodes might promote the removal of phenanthrene from medium by stimulating bacteria and C23O activities.

References (27)

D M K Bird et al.
Interactions between bacteria and plant-parasitic nematodes: now and then
Int J Parasitol
(2003)
D Djigal et al.
Shifts in size, genetic structure and activity of the soil denitrifier community by nematode grazing
Eur J Soil Biol
(2010)
D Djigal et al.
Influence of bacterial-feeding nematodes (Cephalobidae) on soil microbial communities during maize growth
Soil Biol Biochem
(2004)
H Ferris et al.
Structural and functional succession in the nematode fauna of a soil food web
Appl Soil Ecol
(2003)
A K Haritash et al.
Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review
J Hazard Mater
(2009)
P F Landrum et al.
Bioaccumulation and critical body residue of PAHs in the amphipod, Diporeia spp.: additional evidence to support toxicity additivity for PAH mixtures
Chemosphere
(2003)
R G Mattison et al.
The predatory soil flagellate Heteromita globosa stimulates toluene biodegradation by a Pseudomonas sp
Fems Microbiol Lett
(2001)
K A Salinas et al.
Bacterial preferences of the bacterivorous soil nematode Cephalobus brevicauda (Cephalobidae): Effect of bacterial type and size
Pedobiologia
(2007)
L Tian et al.
Kinetics and key enzyme activities of phenanthrene degradation by Pseudomonas mendocina
Process Biochem
(2002)
X Z Yu et al.
Enhanced dissipation of PAHs from soil using mycorrhizal ryegrass and PAH-degrading bacteria
J Hazard Mater
(2011)

S Y Yuan et al.

Biodegradation of phenanthrene in river sediment

Chemosphere

(2001)

T Assefa et al.

Evaluation of the modified Baermann's method in the laboratory diagnosis of Strongyloides stercoralis

Ethio Med J

(1991)

M Bouchez et al.

Les hydrocarbures aromatiques polycycliques dans l'environnement. Première partie. Propriété, origines, devenir?

Oil Gas Sci Technol (in French)

(1996)

Cited by (7)

Oil degradation and variation of microbial communities in contaminated soils induced by different bacterivorous nematodes species
2022, Ecotoxicology and Environmental Safety
Citation Excerpt :
In addition to their own metabolism, nematodes also affect soil energy flow and the soil ecosystem through direct or indirect effects on soil bacteria (Yeates and Bird, 1994; Yeates and Bongers, 1999). Inoculation of soils with bacterivorous nematodes can multiply soil bacteria and boost their activities, thereby promoting the release of CO2, making Gram-positive and -negative bacteria, actinomycetes, and fungi in soil thrive, which changed the structure of the soil microbial community, and consequently contributed to the mineralization and degradation of soil organic matters (Chen et al., 2004; Jing et al., 2017). The mechanisms by which bacterivorous nematodes stimulate the amount and activity of soil bacteria could be the following: (1) the secretions and excretions produced by nematodes contain substances that can provide nutrients for bacteria and therefore stimulate bacterial growth; (2) most of the bacteria that nematodes feed on remain active after passing through the intestinal tract of nematodes, and some bioactive substances and nutrients may be obtained in the intestinal tract to increase their activity; (3) nematodes have strong mobility and can carry microorganisms to areas where nutrients are rich but inaccessible to microorganisms (Griffiths and Bardgett, 1997; Mamilov et al., 2001; Zhou, 2011).
Oil pollution poses a great threat to environments and makes the remediation of oil-contaminated soils an urgent task. Microorganisms are the main biological factor for oil removal in the environment but microbial remediation is greatly affected by environmental factors. For our research, we inoculated three species of bacterivorous nematodes into oil-contaminated soil to explore how bacterivorous nematodes affect soil microbial activities and community structure in contaminated soil, as well as how efficiently different nematodes remove oil pollution from the soil. Six treatments were set in this experiment: sterilized oil-contaminated soil (SOC); nematode-free soil (S); oil-contaminated soil (OC); oil-contaminated soil + Caenorhabditis elegans (OCN1); oil-contaminated soil + Cephalobus persegnis (OCN2); oil-contaminated soil + Rhabditis marina (OCN3) for a 168-day incubation experiment. After the experiment was done, the oil contents in SOC, OC, OCN1, OCN2, and OCN3 were reduced by 6.5%, 32.3%, 38.2%, 42.8%, and 40.2%, respectively, compared with the beginning of the experiment. The amount of phospholipid fatty acids (PLFAs) of Gram-negative bacteria in OC, OCN1, OCN2, and OCN3 was increased by 50.9%, 43.4%, 37.7%, and 47.9%, respectively, compared with that of S. During the 168-day incubation period, the maximum growth of the number of nematodes in OCN1, OCN2, and OCN3 compared with the initial number of the nematodes were 2.25-, 1.52-, and 1.65-fold, respectively. The amount of oil residue in the contaminated soil negatively correlated with the populations of nematodes, total microorganisms, Gram-negative bacteria, actinomycetes, and eukaryotes. Thus, oil pollution increased the number of Gram-negative bacteria, decreased the ratio of Gram-positive bacteria/Gram-negative bacteria and Fungi/Bacteria significantly, and altered the community structure of soil microorganisms. Each species of bacterivorous nematodes has got its unique effect on the microbial activity and community structure in oil contaminated soils, but those tested can promote oil degradation and thus improve the environment of oil contaminated soils.
Effects of bacterial-feeding nematodes on soil microbial activity and the microbial community in oil-contaminated soil
2019, Journal of Environmental Management
Citation Excerpt :
A number of studies have reported that bacterial-feeding nematodes can promote soil organic matter degradation, enhance nutrient mineralization, accelerate plant growth (Hubas et al., 2010; Wu et al., 2005). For example, nematodes have been shown to increase the soil microbial biomass carbon, nitrogen and phosphorus (Chen et al., 2004), enhance soil microbial activity (Jing et al., 2017) and modify the composition of the microbial community structure (Djigal et al., 2010; Xiao et al., 2010). Several studies have demonstrated that nematodes also exist widely in contaminated soils, including oil-contaminated soil, with bacterial-feeding nematodes being the most abundant in these types of soils (García-Segura et al., 2018; Leite et al., 2014; Louati et al., 2015).
Rapid economic development has caused an increase in serious pollution problems due to the ever-increasing use of oil and its products, thus making oil pollution control an urgent task. Studies have shown that large amounts of bacterial-feeding nematodes are present in oil-contaminated soil; their function is as yet unclear. In this experiment, different densities of Caenorhabditis elegans (C. elegans) were inoculated into artificially simulated oil-contaminated soil to examine their effects on microbial activity and the microbial community in oil-contaminated soil. Six treatments were investigated: sterilized oil-contaminated soil as control 1 (FSP), nematode-free soil as control 2 (S), oil-contaminated soil (SP), oil-contaminated soil + 5, 10 or 20 individual C. elegans per gram of dry soil (i.e., SPN5, SPN10, SPN20). Results showed that oil pollution significantly increased the soil basal respiration. However, C. elegans weakened the soil basal respiration to different degrees and soil microbial respiration entropy essentially changed in line with the soil basal respiration. Oil pollution and C. elegans boosted catalase activity in contaminated soil by approximately 64.2–145.1%. Soil urease activity of SPN5, SPN10 and SPN20 was 88.5%, 126.7% and 109.0% stronger, respectively, than that of SP. The inoculation of C. elegans changed the microbial phospholipid fatty acid content in the oil-contaminated soil, including soil bacteria, fungi, actinomycetes, Gram-positive bacteria (G⁺) and Gram-negative bacteria (G⁻). Therefore, this research demonstrates that C. elegans can stimulate microbial reproduction in oil-contaminated soil, enhance related soil enzyme activities and regulate soil microbial community structure and diversity, thereby improving the contaminated soil environment and promoting oil degradation.
Soil fauna-microbial interactions shifts fungal and bacterial communities under a contamination disturbance
2023, PLoS ONE
Co-metabolic Effect of Glucose on Methane Production and Phenanthrene Removal in an Enriched Phenanthrene-Degrading Consortium Under Methanogenesis
2021, Frontiers in Microbiology
Earthworms and rice straw enhanced soil bacterial diversity and promoted the degradation of phenanthrene
2020, Environmental Sciences Europe
Effects of different speices of bacterial-feeding nematodes on soil microorganisms in oil-contaminated soils
2020, Zhongguo Huanjing Kexue/China Environmental Science

View all citing articles on Scopus

View full text

Article preview

Pedosphere

Abstract

References (27)

Interactions between bacteria and plant-parasitic nematodes: now and then

Int J Parasitol

Shifts in size, genetic structure and activity of the soil denitrifier community by nematode grazing

Eur J Soil Biol

Influence of bacterial-feeding nematodes (Cephalobidae) on soil microbial communities during maize growth

Soil Biol Biochem

Structural and functional succession in the nematode fauna of a soil food web

Appl Soil Ecol

Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review

J Hazard Mater

Bioaccumulation and critical body residue of PAHs in the amphipod, Diporeia spp.: additional evidence to support toxicity additivity for PAH mixtures

Chemosphere

The predatory soil flagellate Heteromita globosa stimulates toluene biodegradation by a Pseudomonas sp

Fems Microbiol Lett

Bacterial preferences of the bacterivorous soil nematode Cephalobus brevicauda (Cephalobidae): Effect of bacterial type and size

Pedobiologia

Kinetics and key enzyme activities of phenanthrene degradation by Pseudomonas mendocina

Process Biochem

Enhanced dissipation of PAHs from soil using mycorrhizal ryegrass and PAH-degrading bacteria

J Hazard Mater

Biodegradation of phenanthrene in river sediment

Chemosphere

Evaluation of the modified Baermann's method in the laboratory diagnosis of Strongyloides stercoralis

Ethio Med J

Les hydrocarbures aromatiques polycycliques dans l'environnement. Première partie. Propriété, origines, devenir?

Oil Gas Sci Technol (in French)

Cited by (7)

Oil degradation and variation of microbial communities in contaminated soils induced by different bacterivorous nematodes species

Effects of bacterial-feeding nematodes on soil microbial activity and the microbial community in oil-contaminated soil

Soil fauna-microbial interactions shifts fungal and bacterial communities under a contamination disturbance

Co-metabolic Effect of Glucose on Methane Production and Phenanthrene Removal in an Enriched Phenanthrene-Degrading Consortium Under Methanogenesis

Earthworms and rice straw enhanced soil bacterial diversity and promoted the degradation of phenanthrene

Effects of different speices of bacterial-feeding nematodes on soil microorganisms in oil-contaminated soils