Skip to main content
SpringerLink
Log in

Coprinus comatus endophytic bacteria characteristics and mechanisms for the cadmium resistance

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Characteristics and resistant mechanisms of macro-fungus endophytic bacteria to cadmium (Cd) have not been well defined. Strains L1 and L3 with Cd-resistant capacity were isolated from the fruiting body of Coprinus comatus, which were identified as Bacillus sp. Under the stress of Cd, the morphologies of both L1 and L3 changed to reduce the threat of Cd. The results of Fourier Transform Infrared Spectrometry indicated that functional groups such as –OH, -COOH, and –NH2 participated in the Cd adsorption process. The contents of Cd adsorbed on the cell wall of L1 were 83.46–174.51% higher than that of L3. On the contrary, the contents of Cd accumulated in L1 cytoplasm were 38.77–74.77% lower than that of L3. As the level of Cd increased from 10 to 30 mg/L, the percentages of Cd distributed on the cell walls of L1 and L3 increased by 42.43% and 26.78%, respectively. The results also revealed that the contents of Cd absorbed by the sterilized strains L1 and L3 were 47.67–64.94% and 8.65–78.63% higher than that of living ones, respectively. In addition, the proline production of L1 was 23.75–109.68% higher than that of L3, while the malondialdehyde (MDA) production of L1 was 0.96–15.60% lower than that of L3. Thus, through the comparison of endophytic bacterial physiological responses, the possible characteristics and resistant mechanisms of macro-fungus endophytic bacteria under Cd stress were firstly reported.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Ahemad M (2012) Implications of bacterial resistance against heavy metals in bioremediation: a review. IIOAB J 3:39–46

    CAS  Google Scholar 

  • Babu AG, Kim JD, Oh BT (2013) Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. J Hazard Mater 250-251:477–483

    CAS  Google Scholar 

  • Bayramoğlu G, Arıca MY (2008) Removal of heavy mercury(II), cadmium(II) and zinc(II) metal ions by live and heat inactivated Lentinus edodes pellets. Chem Eng J 143:133–140

    Google Scholar 

  • Blackmore G, Wang W-X (2004) The transfer of cadmium, mercury, methylmercury, and zinc in an intertidal rocky shore food chain. J Exp Mar Biol Ecol 307:91–110

    CAS  Google Scholar 

  • Choudhary M, Jetley UK, Khan MA, Zutshi S, Fatma T (2007) Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotoxicol Environ Saf 66:204–209

    CAS  Google Scholar 

  • Collin-Hansen C, Andersen RA, Steinnes E (2005) Damage to DNA and lipids in Boletus edulis exposed to heavy metals. Mycol Res 109:1386–1396

    CAS  Google Scholar 

  • Costa JM, Loper JE (1994) Characterization of siderophore production by the biological control agent Enterobacter cloacae. Mol Plant-Microbe Interact 7:440–448

    CAS  Google Scholar 

  • Doyle RJ, Matthews TH, Streips UN (1980) Chemical basis for selectivity of metal ions by the Bacillus subtilis cell wall. J Bacteriol 143:471–480

    CAS  Google Scholar 

  • El-Enany AE, Issa AA (2001) Proline alleviates heavy metal stress in Scenedesmus armatus. Folia Microbiol 46:227–230

    CAS  Google Scholar 

  • Farago ME, Mullen WA (1979) Plants which accumulate metals. Part IV. A possible copper-proline complex from the roots of armeria maritima. Inorg Chim Acta 32:L93–L94

    CAS  Google Scholar 

  • Gautam PAS, Pennathur (2017) Studies on the biofilm produced by Pseudomonas aeruginosa grown in different metal fatty acid salt media and its application in biodegradation of fatty acids and bioremediation of heavy metal ions. Can J Microbiol 63:61–73

    Google Scholar 

  • Ge Z, Pei H, Wang L, Song S, Fan C (2011) Electrochemical single nucleotide polymorphisms genotyping on surface immobilized three-dimensional branched DNA nanostructure. SCIENCE CHINA Chem 54:1273–1276

    CAS  Google Scholar 

  • Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. J Occup Med Toxicol 1:22

    Google Scholar 

  • Guo H, Luo S, Chen L, Xiao X, Xi Q, Wei W, Zeng G, Liu C, Wan Y, Chen J, He Y (2010) Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14. Bioresour Technol 101:8599–8605

    CAS  Google Scholar 

  • Gurbanov R, Simsek Ozek N, Gozen AG, Severcan F (2015) Quick discrimination of heavy metal resistant bacterial populations using infrared spectroscopy coupled with chemometrics. Anal Chem 87:9653–9661

    CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 366:1–11

    Google Scholar 

  • Hallmann J, Mahaffee WF, Kloepper JW, Quadthallmann A (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914

    CAS  Google Scholar 

  • Harrison JJ, Ceri H, Turner RJ (2007) Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5:928–938

    CAS  Google Scholar 

  • Hmida-Sayari A, Gargouri-Bouzid R, Bidani A, Jaoua L, Savouré A, Jaoua S (2005) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers salt tolerance in transgenic potato plants. Plant Sci 169:746–752

    CAS  Google Scholar 

  • Jiang J, Liu H, Li Q, Gao N, Yao Y, Xu H (2015) Combined remediation of Cd–phenanthrene co-contaminated soil by Pleurotus cornucopiae and Bacillus thuringiensis FQ1 and the antioxidant responses in Pleurotus cornucopiae. Ecotoxicol Environ Saf 120:386–393

    CAS  Google Scholar 

  • Jouili H, Ferjani EE (2003) Changes in antioxidant and lignifying enzyme activities in sunflower roots (Helianthus annuus L.) stressed with copper excess. C R Biol 326:639–644

    CAS  Google Scholar 

  • Lee S, Flores-Encarnación M, Contreras-Zentella M, Garcia-Flores L, Kennedy C (2004) Indole-3-acetic acid biosynthesis is deficient in Gluconacetobacter diazotrophicus strains with mutations in cytochrome c Biogenesis Genes. J Bacteriol 186:5384–5391

    CAS  Google Scholar 

  • Lemire JA, Harrison JJ, Turner RJ (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11:371–384

    CAS  Google Scholar 

  • Liu HL, Chen BY, Lan YW, Cheng YC (2004) Biosorption of Zn(II) and Cu(II) by the indigenous Thiobacillus thiooxidans. Chem Eng J 97:195–201

    CAS  Google Scholar 

  • Ma Y, Prasad MNV, Rajkumar M, Freitas HJBA (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258

    CAS  Google Scholar 

  • Ma L, Peng Y, Wu B, Lei D, Xu H (2013) Pleurotus ostreatus nanoparticles as a new nano-biosorbent for removal of Mn(II) from aqueous solution. Chem Eng J 225:59–67

    CAS  Google Scholar 

  • Malik A (2004) Metal bioremediation through growing cells. Environ Int 30:261–278

    CAS  Google Scholar 

  • Manasi, Rajesh N, Rajesh V (2016) Evaluation of the genetic basis of heavy metal resistance in an isolate from electronic industry effluent. J Genet Eng Biotechnol 14:177–180

    CAS  Google Scholar 

  • Manisha N, Vinod K, Sharma (2019) Multimetal tolerance mechanisms in bacteria: the resistance strategies acquired by bacteria that can be exploited to 'clean-up' heavy metal contaminants from water. Aquat Toxicol 212:1–10

    Google Scholar 

  • Mastretta C, Taghavi S, van der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11:251–267

    CAS  Google Scholar 

  • Nepple BB, Flynn I, Bachofen R (1999) Morphological changes in phototrophic bacteria induced by metalloid oxyanions. Microbiol Res 154:191–198

    CAS  Google Scholar 

  • Neumann G, Veeranagouda Y, Karegoudar TB, Sahin Ö, Mäusezahl I, Kabelitz N, Kappelmeyer U, Heipieper HJ (2005) Cells of Pseudomonas putida and Enterobacter sp. adapt to toxic organic compounds by increasing their size. Extremophiles 9:163–168

    CAS  Google Scholar 

  • Nikolopoulos D, Manetas Y (1991) Compatible solutes and in vitro stability of Salsola soda enzymes: proline incompatibility. Phytochemistry 30:411–413

    CAS  Google Scholar 

  • Panwichian S, Kantachote D, Wittayaweerasak B, Mallavarapu M (2011) Removal of heavy metals by exopolymeric substances produced by resistant purple nonsulfur bacteria isolated from contaminated shrimp ponds. Electron J Biotechnol 14:2

    Google Scholar 

  • Pospíšil P, Prasad A, Rác M (2019) Mechanism of the formation of electronically excited species by oxidative metabolic processes: role of reactive oxygen species. Biomolecules 9:258

    Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    CAS  Google Scholar 

  • Rita et al (2007) Isolation and characterization of endophytic bacteria from the nickel hyperaccumulator plant Alyssum bertolonii. Microb Ecol 53:306–316

    Google Scholar 

  • Sánchez C (2017) Reactive oxygen species and antioxidant properties from mushrooms. Synth Syst Biol 2:13–22

    Google Scholar 

  • Schulz B, Wanke U, Draeger S, Aust H-J (1993) Endophytes from herbaceous plants and shrubs: effectiveness of surface sterilization methods. Mycol Res 97:1447–1450

    Google Scholar 

  • Schutzendubel A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    CAS  Google Scholar 

  • Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144

    CAS  Google Scholar 

  • Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170

    CAS  Google Scholar 

  • Sriram MI, Kalishwaralal K, Deepak V, Gracerosepat R, Srisakthi K, Gurunathan S (2011) Biofilm inhibition and antimicrobial action of lipopeptide biosurfactant produced by heavy metal tolerant strain Bacillus cereus NK1. Colloids Surf B: Biointerfaces 85:174–181

    CAS  Google Scholar 

  • Tan H, Wang C, Zeng G, Luo Y, Li H, Xu H (2019) Bioreduction and biosorption of Cr(VI) by a novel Bacillus sp. CRB-B1 strain. J Hazard Mater 386:121628

    Google Scholar 

  • Tarley CRT, Arruda MAZ (2004) Biosorption of heavy metals using rice milling by-products. Characterisation and application for removal of metals from aqueous effluents. Chemosphere 54:987–995

    Google Scholar 

  • Troll W, Lindsley J (1955) A photometric method for the determination of proline. J Biol Chem 215:655–660

    CAS  Google Scholar 

  • Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91:127–141

    CAS  Google Scholar 

  • Wang S, Wan C, Wang Y, Chen H, Zhou Z, Fu H, Sosebee R (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert. China J Arid Environ 56:525–539

    Google Scholar 

  • Wang Y, Zhang B, Chen N, Wang C, Feng S, Xu H (2017) Combined bioremediation of soil co-contaminated with cadmium and endosulfan by Pleurotus eryngii and Coprinus comatus. J Soils Sediments 18:2136–2147

    Google Scholar 

  • Wang Y, Wang X, Lan W, Wei Y, Xu H (2021) Impacts and tolerance responses of Coprinus comatus and Pleurotus cornucopiae on cadmium contaminated soil. Ecotoxicol Environ Saf 211:111929

    CAS  Google Scholar 

  • Wei B, Yang L (2010) A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchem J 94:99–107

    CAS  Google Scholar 

  • Wu B, Wang Z, Zhao Y, Gu Y, Wang Y, Yu J, Xu H (2019) The performance of biochar-microbe multiple biochemical material on bioremediation and soil micro-ecology in the cadmium aged soil. Sci Total Environ 686:719–728

    CAS  Google Scholar 

  • Xie X, Yu C, Ma D (2006) Enantioselective arylation of 2-methylacetoacetates catalyzed by CuI/trans-4-hydroxy-L-proline at low reaction temperatures. J Am Chem Soc 128:16050–16051

    CAS  Google Scholar 

  • Y.M. Hua YXC, Zhang SH (2011) Variation in sulfur bacteria and extracellular polymeric substances during sewage sludge bioleaching. China Environ Sci 31:795–802

    Google Scholar 

  • Yan L et al (2010) Seedlings growth and antioxidative enzymes activities in leaves under heavy metal stress differ between two desert plants: a perennial (Peganum harmala) and an annual (Halogeton glomeratus) grass. Acta Physiol Plant 32:583–590

    Google Scholar 

  • Yunchuan L, Zhao Q, Cheng G, Xu H (2011) Exploring the mechanism of lead(II) adsorption from aqueous solution on ammonium citrate modified spent Lentinus edodes. Chem Eng J 173:792–800

    Google Scholar 

  • Zeng FX, Jiang H, Zhang XS (2011) Adsorption of lead (Pb) from aqueous solution with Typha angustifolia biomass modified by SOCl2 activated EDTA. Chem Eng J 170:21–28

    Google Scholar 

  • Zhang J, Kirkham MB (1993) Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791

    Google Scholar 

Download references

Acknowledgements

The authors wish to thank Professor Guanglei Cheng and Hui Wang from the Sichuan University for the technical assistance.

Funding

This study was financially supported by the Regional Innovation Cooperation Project of Sichuan Province (2021YFQ0014) and the Fundamental Research Funds for the Central Universities (SCU2019D013).

Author information

Authors and Affiliations

  1. Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, No.24 South Section 1, Yihuan Road, Chengdu, 610065, Sichuan, People’s Republic of China

    Ying Wang, Huanyan Luo, He Peng, Xitong Wang, Fei Xu & Heng Xu

Authors
  1. Ying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huanyan Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. He Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xitong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Ying Wang: conceptualization, investigation, methodology, data curation, writing original draft, and writing—review and editing. Huanyan Luo: conceptualization, investigation, methodology, and writing—review and editing. He Peng: methodology and data curation. Xitong Wang: investigation and methodology. Fei Xu: software, investigation, and visualization. Heng Xu: writing—review and editing.

Corresponding author

Correspondence to Heng Xu.

Ethics declarations

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent to publish

All authors whose names appear on the submission approved the version to be published and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Competing interests

The authors declare no competing interests.

Additional information

Responsible editor: Gangrong Shi

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, ., Luo, H., Peng, H. et al. Coprinus comatus endophytic bacteria characteristics and mechanisms for the cadmium resistance. Environ Sci Pollut Res 29, 584–593 (2022). https://doi.org/10.1007/s11356-021-15381-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-15381-5

Keywords

Search

Navigation