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Environmental pollutants, pathogens and immune system in earthworms

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Shyamasree Ghosh
Shyamasree Ghosh
Shyamasree Ghosh
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Abstract and Figures

Earthworms also known as farmer’s friends are natural tillers of soil. They belong to Phylum Annelida and class Oligochaeta. Acid soils with organic matter and surface humus maintain the largest fauna of worms and earthworms. Due to their habitat in soil, they are constantly exposed to microbes and pollution generated by anthropogenic sources. Studies have revealed that damage of the immune system of earthworms can lead to alterations of both morphological and cellular characteristics of worms, activation of signalling pathways and can strongly influence their survival. Therefore, the understanding of the robust immune system in earthworms has become very important from the point of view of understanding its role in combating pathogens and pollutants and its role in indicating the soil pollution. In this article, we have outlined the (i) components of the immune system and (ii) their function of immunological responses on exposure to pollutants and pathogens. This study finds importance from the point of view of ecotoxicology and monitoring of earthworm health and exploring the scope of earthworm immune system components as biomarkers of pollutants and environmental toxicity. The future scope of this review remains in understanding the earthworm immunobiology and indicating strong biomarkers for pollution.
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REVIEW ARTICLE
Environmental pollutants, pathogens and immune
system in earthworms
Shyamasree Ghosh
1,2
Received: 30 August 2017 / Accepted: 26 December 2017 / Published online: 11 January 2018
#Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Earthworms also known as farmer’s friends are natural tillers of soil. They belong to Phylum Annelida and class Oligochaeta.
Acid soils with organic matter and surface humus maintain the largest fauna of worms and earthworms. Due to their habitat in
soil, they are constantly exposed to microbes and pollution generated by anthropogenic sources. Studies have revealed that
damage of the immune system of earthworms can lead to alterations of both morphological and cellular characteristics of worms,
activation of signalling pathways and can strongly influence their survival. Therefore, the understanding of the robust immune
system in earthworms has become very important from the point of view of understanding its role in combating pathogens and
pollutants and its role in indicating the soil pollution. In this article, we have outlined the (i) components of the immune system
and (ii) their function of immunological responses on exposure to pollutants and pathogens. This study finds importance from the
point of view of ecotoxicology and monitoring of earthworm health and exploring the scope of earthworm immune system
components as biomarkers of pollutants and environmental toxicity. The future scope of this review remains in understanding the
earthworm immunobiology and indicating strong biomarkers for pollution.
Keywords Earthworm .Annelida .Innate immunity .Ecotoxicology .Biomarkers
Organisms and their abbreviations are studied in the text
Earthworms
A. caliginosa Aporrectodea calignosa
A. tuberculata Aporrectodea tuberculata
D. veneta Dendrobaena veneta
D. rubidus Dendrodrilus rubidus
E. fetida Eisenia fetida
E.f. Andrei Eisenia fetida andrei
E. hortensis Eisenia hortensis
E. veneta Eisenia veneta
E. Andrei Eisenia andrei
E. prashadi Eudichogaster prashadi
E. eugeniae Eudrilus eugeniae
H. diversicolor Hediste diversicolor
L. rubellus Lumbricus rubellus
L. terrestris Lumbricus terrestris
P. sansibaricus Perionyx sansibaricus
P. guillelmi (Michaelsen) Pheretima guillelmi (Michaelsen)
P. tschiliensis Pheretima tschiliensis
Bacteria
Aeromonas Aeromonas
B. subtilis Bacillus subtilis
C. perfringens Clostridium perfringens
C. septicum Clostridium septicum
E. coli Escherichia coli
M. luteus Micrococus luteus
Fungus
S. cerevisiae Saccharomyces cerevisiae
Introduction
Earthworms belonging to the invertebrate phylum Annelida
(Table 1) are also known as Bfarmers friends^that are the
natural tillers of the soil and thus are beneficial for the human
Responsible editor: Philippe Garrigues
*Shyamasree Ghosh
shyamasree_b@yahoo.com; sree.s@niser.ac.in
1
School of Biological Sciences, National Institute of Science
Education and Research (NISER), Bhubaneswar, Odisha 752050,
India
2
Homi Bhabha National Institute, Training School Complex,
Anushakti Nagar, Mumbai 400094, India
Environmental Science and Pollution Research (2018) 25:6196–6208
https://doi.org/10.1007/s11356-017-1167-8
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... SS toxicity to earthworms can be caused by various pollutants. Generally, earthworms are very sensitive to elevated concentrations of ammonia (Domínguez, 2004), heavy metals (Natal-da-Luz et al., 2009), and pathogens (Ghosh, 2018); however, SS can contain Fig. 4. MDA concentrations in earthworm tissue. The letters above the columns represent significant differences for each WWTP (P < 0.05). ...
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... They belong to the phylum Annelida, subclass Oligochaeta (PIEARCE et al., 1990). these organisms act as natural plows for the soil and produce vermicompost (Antunes et al, 2021), which is a highly valuable material for meeting the nutritional needs of crops (GHOSH, 2018;ASLAM et al., 2021). ...
EFFECT OF THE BALANCED AND NANO-COMPOSITE NPK FERTILIZER ON THE VITALITY OF THE EARTHWORM Octolasion cyanieum AND ITS EFFECT ON THE HISTOLOGICAL COMPOSITION OF THE MIDDLE OF THE BODY
Article
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This study was conducted to determine the effects of earthworm breeding O. cyanieum for 7, 14, 21, and 28 days in soil treated with concentrations of 800, 1000, 1500, and 2000 mg kg-1 of balanced NPK compound fertilizer and balanced NPK nano-compound fertilizer at concentrations of 30, 60, 120, and 240 mg kg-1, in addition to the control treatment. It was found that the weight and relative growth rate of earthworms decreased with increasing concentrations of fertilizers. The highest significant decrease in weight (0.257 g) and relative growth rate (40.34%) was observed at a concentration of 1500 mg kg-1 of balanced NPK compound fertilizer. Meanwhile, the highest decrease in worm weight (0.225 g) and relative growth rate (86.31%) was observed at a concentration of 240 mg kg-1 of balanced NPK nano-compound fertilizer. Fertilizers also affected the protein content in the earthworms, which differed significantly from the control treatment for both fertilizers. In addition, the fertilizers affect the histological structure of the body, with clear disruption in the epithelium of the body, layers of circular and longitudinal muscle, the lining of the intestine, especially the typhlosole. Keywords: chemical fertilizer; nano fertilizer; earthworm vitality. Efeito do fertilizante npk balanceado e nanocomposto na vitalidade da minhoca octolasion cyanieum e seu efeito na composição histológica do meio do corpo RESUMO: Este estudo foi conduzido para determinar os efeitos da criação de minhocas O. cyanieum por 7, 14, 21 e 28 dias em solo tratado com concentrações de 800, 1000, 1500 e 2000 mg kg-1 de solo de fertilizante composto NPK balanceado (20-20-20) e fertilizante nanocomposto NPK balanceado (20-20-20) nas concentrações de 30, 60, 120 e 240 mg kg-1 de solo, além do tratamento testemunha. O estudo mostrou que os fertilizantes químicos tiveram impacto sobre a vitalidade dessas minhocas, pois o peso e a taxa de crescimento relativo das minhocas diminuíram com o aumento das concentrações de fertilizantes. A maior queda significativa no peso (0,257 g) e na taxa de crescimento relativo (40,34%) foi observada na concentração de 1500 mg kg-1 de solo do fertilizante composto NPK balanceado. Já a maior redução no peso (0,225 g) e na taxa de crescimento relativo (86,31%) da minhoca foi observada na concentração de 240 mg kg-1 de solo do fertilizante nanocomposto NPK balanceado. Além disso, os tratamentos acima tiveram impacto no teor de proteína dos corpos das minhocas, que diferiu significativamente do tratamento controle, para ambos os tipos de fertilizantes. O estudo mostrou o impacto do fertilizante nas estruturas dos tecidos das minhocas, com clara ruptura na camada da pele e nas camadas musculares circulares e longitudinais abaixo dela, bem como um claro efeito no revestimento intestinal, especialmente o tiflosole. Palavras-chave: fertilizante químico; nano fertilizante; vitalidade da minhoca.
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... Studies in molecular biology, biochemistry and transcriptome with deep sequencing approaches have enabled the understanding of the robust immune system in earthworms which is significant from the eco-toxicology point of view. For a greater understanding of the robust nature of the earthworm immune system we direct the readers to refer (GHOSH, 2018). The vast number of species and their importance both from the economic and ecotoxicology point of view have enabled them to be important organisms of study. ...
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Study of Earthworm Metabolites Using GC–MS and FT-IR Based Approaches
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  • Apr 2024
Earthworms, by their soil-dwelling nature, feeding and burrowing activity in the soil, are known to increase soil fertility and are also referred as nature's plough by Charles Darwin. They ingest organic matter from the soil, are exposed to microbes and pollutants, and excrete casts in the soil adding to the soil fertility. Although earthworms are essential for soil mineralisation process, their metabolism and impact on environment are not well studied. In this study, we investigated the gut voided biochemical constituents of Lampito mauritii (L. mauritii) and analyzed by FT-IR and GC–MS studies. The results indicated significant findings, including identification of unique biochemical components with 16 major compounds in L. mauritii with a significant peak at retention time 4.09 and other peaks at 4.13, 4.27, 4.53, 4.88, 5.44, 7.21 and 16.49 revealed by GC–MS analysis Our study highlights the expression of unique compounds in the earthworm. It emphasises that metabolism may play a predominant role in altering ingested components of soil organic matter, and the earthworm casts may have a positive impact on the environment.
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Insight into Bioaccumulation of Decabromodiphenyl Ethane in Eisenia fetida Increased by Microplastics
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The rise of electronics inevitably induced the co-pollution of novel brominated flame retardants (NBFRs) and microplastics (MPs). However, studies on how they interact to influence their bioavailability are scarce. Here, we explored the influence mechanism of acrylonitrile butadiene styrene (ABS)-MPs on the bioaccumulation of decabromodiphenyl ethane (DBDPE) in soil-earthworm microcosms. The influence exhibited a temporal pattern characterized by short-term inhibition and long-term promotion. After 28 days of exposure, DBDPE bioaccumulation in a co-exposure (10 mg kg-1 DBDPE accompanied by 1000 mg kg-1 ABS-MPs) was 2.61 times higher than that in a separate exposure. The adsorption process in the soil, intestines, and mucus introduced DBDPE-carried MPs, which had a higher concentration of DBDPE than the surrounding soil and directly affected the bioavailability of DBDPE. MP-pre-exposure (100, 1000, and 10000 mg kg-1) reduced epidermal soundness, mucus secretion, and worm cast production. This eventually promoted the contact between earthworm and soil particles and enhanced the DBDPE of earthworm tissue by 6%-61% in the next DBDPE-postexposure period, confirming that MPs increased DBDPE bioaccumulation indirectly by impairing the earthworm health. This study indicates that MPs promoted DBDPE bioaccumulation via adsorption and self-toxicity, providing new insight into the combined risk of MPs and NBFRs.
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Innovative accumulative risk assessment strategy of co-exposure of As and Pb in medical earthworms based on in vivo-in vitro correlation
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Cryo-EM structure of lysenin pore elucidates membrane insertion by an aerolysin family protein
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Effective activation of antioxidant system by immune-relevant factors reversely correlates with apoptosis of Eisenia andrei coelomocytes
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Earthworms for monitoring metal contamination
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Earthworms are widely used to assess the bioavailability and deleterious effects of metals in contaminated soils. This book discusses some of the direct and indirect methods that have recently been used to determine the ligand-binding speciation and the extent of the toxicologically-important bio-reactive metal and metalloid fractions in the cells of earthworms as receptor organisms. It proceeds to describe suites of cell-based biomarkers (e.g. morphometrics; neutral red retention time and immuno-competence assays), and their variants, that are more-or-less widely used for reporting chemically-evoked stress in earthworms under laboratory, semi-field, and field exposure conditions. NMR-based metabonomic profiling of the tissues of stressed earthworms is reviewed, and the potential of infra-red microspectroscopy for determining the biochemical profiles of specific cells in different functional states is highlighted. The way that the rapidly expanding genomic database is beginning to inform and propel research designed to further understanding of the fundamental mechanisms underpinning metal trafficking and toxicosis at the level of cells, partly through the provision of immuno-histochemical and in situ hybridization ‘tools’, is discussed. The book concludes with the prediction that the future will see the adoption of high-throughput cellular, as well as molecular-genetic, biomarker techniques in earthworm ecotoxicology, possibly with parallel metal fractionation measurements done as a desirable component of experimental design.
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Mode of action of Cr(VI) in immunocytes of earthworms: Implications for animal health
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Chromium (Cr) is one of the major and most detrimental pollutant, widely present in the environment as a result of several anthropogenic activities. In mammalian cells, Cr(VI) is known to enhance reactive oxygen species (ROS) production and to cause toxic and genotoxic effects. Less commonly investigated are the effects and mode of action of this contaminant in invertebrates, particularly in soil organisms. In this work, earthworms of the species Eisenia andrei were exposed for 1 and 3 days to various sublethal concentrations of Cr(VI) (2, 15, 30µgmL(-1)) using the paper contact toxicity test. In amoeboid leukocytes we investigated intracellular ROS and lipoperoxide production, oxidative DNA damage, and the effects on different cell functions. The analysis of the results shows that Cr(VI) triggered severe adverse reactions; the first events were an increase of intracellular ROS levels, generating in the cells oxidative stress conditions leading to membrane lipid peroxidation and oxidative DNA damage. Lysosomes showed relevant changes such as a strong membrane destabilization, which was accompanied by an increased catabolism of cytoplasmic proteins and accumulation of lipofuscin. With an increase in the dose and/or time of exposure, the physiological status of intracellular organelles (such as lysosomes, nucleus and mitochondria) showed further impairment and amoebocyte immune functions were adversely affected, as shown by the decrease of the phagocytic activity. By mapping the responses of the different parameters evaluated, diagnostic of (oxidative) stress events, against lysosomal membrane stability, a "health status" indicator (able to describe the stress syndrome from its early phase to pathology), we have shown that this biomarker is suitable as a prognostic test for health of earthworms. This is viewed as a crucial step toward the derivation of explanatory frameworks for prediction of pollutant impact on animal health.
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Lysenin family proteins in earthworm coelomocytes - Comparative approach
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Sphingomyelin-binding proteins of the lysenin family were originally identified in earthworms belonging to the genus Eisenia comprised of at least two distinct species, E. andrei and E. fetida, until recently considered subspecies or morphotypes of E. foetida (sic). In the present study the presence of lysenin and lysenin-related protein 2 (LRP-2, known also as fetidin) was detected in coelomocytes retrieved from all investigated adult specimens of E. andrei, and E. fetida. They were accompanied by LRP-3 and LRP-1 in some specimens of E. andrei and E. fetida, respectively. Lysenins were not observed in a third composting lumbricid species, Dendrobaena veneta, which served as a convenient negative reference for techniques and procedures used in the study. The pore-forming potential of soluble and cellular fractions of coelomic fluid was studied towards sheep red blood cells and sphingomyelin-rich liposomes. After experimental depletion the potential was restored in parallel with restoration of chloragocyte-derived eleocytes in both E. andrei and E. fetida.
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Phenotypic and functional characterization of earthworm coelomocyte subsets: Linking light scatter-based cell typing and imaging of the sorted populations
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Flow cytometry is a common approach to study invertebrate immune cells including earthworm coelomocytes. However, the link between light-scatter- and microscopy-based phenotyping remains obscured. Here we show, by means of light scatter-based cell sorting, both subpopulations (amoebocytes and eleocytes) can be physically isolated with good sort efficiency and purity confirmed by downstream morphological and cytochemical applications. Immunocytochemical analysis using anti-EFCC monoclonal antibodies combined with phalloidin staining has revealed antigenically distinct, sorted subsets. Screening of lectin binding capacity indicated wheat germ agglutinin (WGA) as the strongest reactor to amoebocytes. This is further evidenced by WGA inhibition assays that suggest high abundance of N-acetyl-D-glucosamine in amoebocytes. Post-sort phagocytosis assays confirmed the functional differences between amoebocytes and eleocytes, with the former being in favor of bacterial engulfment. This study has proved successful in linking flow cytometry and microscopy analysis and provides further experimental evidence of phenotypic and functional heterogeneity in earthworm coelomocyte subsets.
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New Aspects of Earthworm Innate Immunity
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The first exploration of earthworm immunity dates back almost the third quarter of a century. Since then, our journey has led to the discovery of several key biomolecules, some of which are common to invertebrates while some are rather specific to annelids. In light of these findings, we present the new aspects of earthworm immunity in an attempt to foresee potential research directions. We begin with a concise introduction before we discuss the newly described earthworm Toll receptors and their implications. Another key protein, lysenin, has historically been a popular target of research, yet its role in immunity remains obscured. We discuss, on the basis of our novel findings, how lysenin contributes to nanoparticle recognition in coelomocytes. The unique and conserved recognition strategies reviewed here have certainly opened up new research avenues and potentially harbor an intriguing clue for better elucidating the vertebrate immune response toward various antigens.
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