Skip to main content
Springer Nature Link
Log in

Metallophores production by bacteria isolated from heavy metal-contaminated soil and sediment at Lerma–Chapala Basin

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Environmental pollution as a result of heavy metals (HMs) is a worldwide problem and the implementation of eco-friendly remediation technologies is thus required. Metallophores, low molecular weight compounds, could have important biotechnological applications in the fields of agriculture, medicine, and bioremediation. This study aimed to isolate HM-resistant bacteria from soils and sediments of the Lerma–Chapala Basin and evaluated their abilities to produce metallophores and to promote plant growth. Bacteria from the Lerma–Chapala Basin produced metallophores for all the tested metal ions, presented a greater production of As3+ metallophores, and showed high HM resistance especially to Zn2+, As5+, and Ni2+. A total of 320 bacteria were isolated with 170 strains showing siderophores synthesis. Members of the Delftia and Pseudomonas genera showed above 92 percent siderophore units (psu) during siderophores production and hydroxamate proved to be the most common functional group among the analyzed siderophores. Our results provided evidence that Lerma–Chapala Basin bacteria and their metallophores could potentially be employed in bioremediation processes or may even have potential for applications in other biotechnological fields.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Acinas SG, Klepac-Ceraj V, Hunt DE et al (2004) Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430:551

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Ahemad M, Khan MS (2012) Effect of fungicides on plant growth promoting activities of phosphate solubilizing Pseudomonas putida isolated from mustard (Brassica compestris) rhizosphere. Chemosphere 86:945–950

  • Aiken AM, Petersen JM, Peyton BM, et al. (2003) Siderophore mediated metal transport in subsurface environments. In: Poster abstract W03-P302, CBE Technical Advisory Conference, Bozeman, MT

  • Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12:39–45

    Article  CAS  Google Scholar 

  • Ali SS, Vidhale NN (2013) Bacterial siderophore and their application: a review. Int J Curr Microbiol Appl Sci 2(12):303–312

    Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881

    Article  CAS  PubMed  Google Scholar 

  • Arnow LE (1937) Colorimetric determination of the components of 3, 4-dihydroxyphenylalanine-tyrosine mixtures. J Biol Chem 118:531–537

    Article  CAS  Google Scholar 

  • Arora NK, Verma M (2017) Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech 7:381

    Article  PubMed  PubMed Central  Google Scholar 

  • Arroyo-Herrera I, Román-Ponce B, Reséndiz-Martínez AL et al (2021) Heavy-metal resistance mechanisms developed by bacteria from Lerma-Chapala basin. Arch Microbiol 203(4):1807–1823

    Article  CAS  PubMed  Google Scholar 

  • Bátka D, Farkas E (2006) Pb (II)-binding capability of aminohydroxamic acids: primary hydroxamic acid derivatives of α-amino acids as possible sequestering agents for Pb (II). J Inorg Biochem 100:27–35

    Article  PubMed  Google Scholar 

  • Beasley FC, Marolda CL, Cheung J et al (2011) Staphylococcus aureus transporters Hts, Sir, and Sst capture iron liberated from human transferrin by Staphyloferrin A, Staphyloferrin B, and catecholamine stress hormones, respectively, and contribute to virulence. Infect Immun 79:2345–2355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biver M, Shotyk W (2012) Stibnite (Sb2S3) oxidative dissolution kinetics from pH 1 to 11. Geochim Cosmochim Acta 79:127–139

  • Braun V, Pramanik A, Gwinner T et al (2009) Sideromycins: tools and antibiotics. Biometals 22:3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6(9):e04691

    Article  PubMed  PubMed Central  Google Scholar 

  • Carlos MHJ, Stefani PVY, Janette AM et al (2016) Assessing the effects of heavy metals in ACC deaminase and IAA production on plant growth-promoting bacteria. Microbiol Res 188–189:53–61. https://doi.org/10.1016/j.micres.2016.05.001

    Article  CAS  PubMed  Google Scholar 

  • Chai L-Y, Wang Y-Y, Yang Z-H et al (2010) Detoxification of chromium-containing slag by Achromobacter sp. CH-1 and selective recovery of chromium. Trans Nonferrous Met Soc China 20:1500–1504

    Article  CAS  Google Scholar 

  • Chen D, Shao Q, Yin L et al (2018) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1945. https://doi.org/10.3389/fpls.2018.01945

    Article  PubMed  Google Scholar 

  • Christenson EA, Schijf J (2011) Stability of YREE complexes with the trihydroxamate siderophore desferrioxamine B at seawater ionic strength. Geochim Cosmochim Acta 75:7047–7062

    Article  CAS  Google Scholar 

  • Chun J, Lee JH, Jung Y et al (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261. https://doi.org/10.1099/ijs.0.64915-0

    Article  CAS  PubMed  Google Scholar 

  • Chun J, Oren A, Ventosa A et al (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466

    Article  CAS  PubMed  Google Scholar 

  • Cloete KJ, Valentine AJ, Stander MA et al (2009) Evidence of symbiosis between the soil yeast Cryptococcus laurentii and a sclerophyllous medicinal shrub, Agathosma betulina (Berg.) Pillans. Microb Ecol 57:624–632

    Article  PubMed  Google Scholar 

  • Cornejo-Garrido H, Fernández-Lomelín P, Guzmán J, Cervini-Silva J (2008) Dissolution of arsenopyrite (FeAsS) and galena (PbS) in the presence of desferrioxamine-B at pH 5. Geochim Cosmochim Acta 72:2754–2766

    Article  CAS  Google Scholar 

  • Csaky TZ (1948) On the estimation of bound hydroxylamine in biological materials. Acta Chem Scand 2:450–454

    Article  CAS  Google Scholar 

  • Dary M, Chamber-Pérez MA, Palomares AJ, Pajuelo E (2010) “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177(1–3):323–330

    Article  CAS  PubMed  Google Scholar 

  • Dave BP, Anshuman K, Hajela P (2006) Siderophores of halophilic archaea and their chemical characterization

  • de Oliveira LF, Elbl P, Navarro BV et al (2017) Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. Tree Physiol 37:116–130

    Article  PubMed  Google Scholar 

  • Deicke M, Mohr JF, Roy S et al (2019) Metallophore profiling of nitrogen-fixing Frankia spp. to understand metal management in the rhizosphere of actinorhizal plants. Metallomics 11:810–821

    Article  CAS  PubMed  Google Scholar 

  • Diagne N, Arumugam K, Ngom M et al (2013) Use of Frankia and actinorhizal plants for degraded lands reclamation. Biomed Res Int 2013:948258

    Article  PubMed  PubMed Central  Google Scholar 

  • Dimkpa C, Svatoš A, Merten D et al (2008) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 54:163–172

    Article  CAS  PubMed  Google Scholar 

  • Dimkpa CO, Merten D, Svatoš A et al (2009) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107:1687–1696

    Article  CAS  PubMed  Google Scholar 

  • D’Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E, Epstein S, Lewis K (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17(3):254–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández LA, Zalba P, Gómez MA, Sagardoy MA (2007) Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biol Fertil Soils 43:805–809

    Article  Google Scholar 

  • Fiedler H-P, Krastel P, Müller J et al (2001) Enterobactin: the characteristic catecholate siderophore of Enterobacteriaceae is produced by Streptomyces species. FEMS Microbiol Lett 196:147–151

    Article  CAS  PubMed  Google Scholar 

  • Ford TE, Ika R, Shine J et al (2000) Trace metal concentrations in Chirostoma sp. from Lake Chapala, Mexico: elevated concentrations of mercury and public health implications. J Environ Sci Health Part A Toxic/hazard Subst Environ Eng 35:313–325. https://doi.org/10.1080/10934520009376973

    Article  Google Scholar 

  • Galtier N, Guoy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogenies. Bioinformatics 12:543

    Article  CAS  Google Scholar 

  • Gamaler E, Glick BR (2011) Mechanisms used by plant growth-promoting bacteria. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer, Berlin, pp 17–46

    Chapter  Google Scholar 

  • Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374. https://doi.org/10.1016/j.biotechadv.2010.02.001

    Article  CAS  PubMed  Google Scholar 

  • Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerra Sierra BE, Muñoz Guerrero J, Sokolski S (2021) Phytoremediation of heavy metals in tropical soils an overview. Sustainability 13:2574

    Article  Google Scholar 

  • Guo H, Yang Y, Liu K et al (2016) Comparative genomic analysis of Delftia tsuruhatensis MTQ3 and the identification of functional NRPS genes for siderophore production. Biomed Res Int 2016:3687619

    Article  PubMed  PubMed Central  Google Scholar 

  • Gupta V, Saharan K, Kumar L, Gupta R, Sahai V, Mittal A (2008) Spectrophotometric ferric ion biosensor from Pseudomonas fluorescens culture. Biotechnol Bioeng 100(2):284–296

    Article  CAS  PubMed  Google Scholar 

  • Hansen AM, Leon-Zavala A, Bravo-Inclan L (1995) Sources of pollution and metal enrichment in sediments of the Lerma-Chapala Basin. Hydraul Eng Mex 10:55–69

    Google Scholar 

  • Hantke K, Nicholson G, Rabsch W, Winkelmann G (2003) Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci 100:3677–3682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harish S, Kavino M, Kumar N et al (2008) Biohardening with plant growth promoting rhizosphere and endophytic bacteria induces systemic resistance against banana bunchy top virus. Appl Soil Ecol 39:187–200

    Article  Google Scholar 

  • Jay JA, Ford TE (2001) Water concentrations, bioaccumulation, and human health implications of heavy metals in Lake Chapala. Lerma-Chapala Watershed. https://doi.org/10.1007/978-1-4615-0545-7_5

    Article  Google Scholar 

  • Kaevska M, Videnska P, Sedlar K, Slana I (2016) Seasonal changes in microbial community composition in river water studied using 454-pyrosequencing. Springerplus 5:409

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan MS, Zaidi A, Wani PA (2007) Role of phosphate-solubilizing microorganisms in sustainable agriculture—a review. Agron Sustain Dev 27:29–43

    Article  Google Scholar 

  • Khan MIR, Nazir F, Asgher M et al (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    Article  CAS  PubMed  Google Scholar 

  • Kraemer SM, Duckworth OW, Harrington JM, Schenkeveld WDC (2015) Metallophores and trace metal biogeochemistry. Aquat Geochem 21:159–195

    Article  CAS  Google Scholar 

  • Kraepiel AML, Bellenger JP, Wichard T, Morel FMM (2009) Multiple roles of siderophores in free-living nitrogen-fixing bacteria. Biometals 22:573–581

    Article  CAS  PubMed  Google Scholar 

  • Kumar KV, Singh N, Behl HM, Srivastava S (2008) Influence of plant growth promoting bacteria and its mutant on heavy metal toxicity in Brassica juncea grown in fly ash amended soil. Chemosphere 72:678–683

    Article  CAS  PubMed  Google Scholar 

  • Kumar V, Menon S, Agarwal H, Gopalakrishnan D (2017) Characterization and optimization of bacterium isolated from soil samples for the production of siderophores. Resour Technol 3:434–439

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404

    Article  CAS  PubMed  Google Scholar 

  • Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18. https://doi.org/10.18637/jss.v025.i01

    Article  Google Scholar 

  • Lhospice S, Gomez NO, Ouerdane L et al (2017) Pseudomonas aeruginosa zinc uptake in chelating environment is primarily mediated by the metallophore pseudopaline. Sci Rep 7:17132

    Article  PubMed  PubMed Central  Google Scholar 

  • Li K, Ramakrishna W (2011) Effect of multiple metal resistant bacteria from contaminated lake sediments on metal accumulation and plant growth. J Hazard Mater 189:531–539

    Article  CAS  PubMed  Google Scholar 

  • Lin Y-T, Lin Y-F, Tsai IJ et al (2019) Structure and diversity of soil bacterial communities in Offshore Islands. Sci Rep 9:4689

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu W, Yang C, Shi S, Shu W (2014) Effects of plant growth-promoting bacteria isolated from copper tailings on plants in sterilized and non-sterilized tailings. Chemosphere 97:47–53

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009) Inoculation of plant growth promoting bacterium Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J Environ Manage 90:831–837

    Article  PubMed  Google Scholar 

  • Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manage 174:14–25

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Rajkumar M, Oliveira RS et al (2019) Potential of plant beneficial bacteria and arbuscular mycorrhizal fungi in phytoremediation of metal-contaminated saline soils. J Hazard Mater 379:120813

    Article  CAS  PubMed  Google Scholar 

  • Manecki M, Maurice PA (2008) Siderophore promoted dissolution of pyromorphite. Soil Sci 173:821–830

  • Mastropasqua MC, D’orazio M, Cerasi M et al (2017) Growth of Pseudomonas aeruginosa in zinc poor environments is promoted by a nicotianamine-related metallophore. Mol Microbiol 106:543–561

    Article  CAS  PubMed  Google Scholar 

  • Maurer B, Muller A, Kellersc W, Zahner H (1968) Ferribactin a siderochrome from Pseudomonas fluorescens migula. Arch Mikrobiol 60:326

    Article  CAS  PubMed  Google Scholar 

  • May JJ, Wendrich TM, Marahiel MA (2001) The dhb operon of Bacillus subtilis Encodes the biosynthetic template for the catecholic siderophore 2, 3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276:7209–7217

    Article  CAS  PubMed  Google Scholar 

  • McRose DL, Seyedsayamdost MR, Morel FMM (2018) Multiple siderophores: bug or feature? J Biol Inorg Chem 23:983–993

    Article  CAS  PubMed  Google Scholar 

  • Mehnaz S, Kowalik T, Reynolds B, Lazarovits G (2010) Growth promoting effects of corn (Zea mays) bacterial isolates under greenhouse and field conditions. Soil Biol Biochem 42:1848–1856

    Article  CAS  Google Scholar 

  • Menéndez AB, Calzadilla PI, Sansberro PA, et al (2019) Polyamines and legumes: Joint stories of stress, nitrogen fixation and environment. PeerJ Preprints

  • Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milner SJ, Seve A, Snelling AM, Thomas GH, Kerr KG, Routledge A, Duhme-Klair AK (2013) Staphyloferrin A as siderophore-component in fluoroquinolone-based Trojan horse antibiotics. Org Biomol Chem 11(21):3461–3468

    Article  CAS  PubMed  Google Scholar 

  • Mishra A, Fischer MKR, Bäuerle P (2009) Metal-free organic dyes for dye-sensitized solar cells: from structure: property relationships to design rules. Angew Chemie Int Ed 48:2474–2499

    Article  CAS  Google Scholar 

  • Moberly JG, Staven ARI, Sani RK, Peyton BM (2010) Influence of pH and inorganic phosphate on toxicity of zinc to Arthrobacter sp. isolated from heavy-metal-contaminated sediments. Environ Sci Technol 44:7302–7308

    Article  CAS  PubMed  Google Scholar 

  • Morel MA, Iriarte A, Jara E et al (2016) Revealing the biotechnological potential of Delftia sp. JD2 by a genomic approach. AIMS Bioeng 3:156–175

    Article  CAS  Google Scholar 

  • Mustafavi SH, Badi HN, Sękara A et al (2018) Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites. Acta Physiol Plant 40:102

    Article  Google Scholar 

  • Nagoba B, Vedpathak D (2011) Medical applications of siderophores. Eur J Gen Med 8(3):229–235

    Google Scholar 

  • Nair A, Juwarkar AA, Singh SK (2007) Production and characterization of siderophores and its application in arsenic removal from contaminated soil. Water Air Soil Pollut 180:199–212

    Article  CAS  Google Scholar 

  • Ngom M, Oshone R, Diagne N et al (2016) Tolerance to environmental stress by the nitrogen-fixing actinobacterium Frankia and its role in actinorhizal plants adaptation. Symbiosis 70:17–29

    Article  CAS  Google Scholar 

  • Nies DH (2000) Heavy metal-resistant bacteria as extremophiles: molecular physiology and biotechnological use of Ralstonia sp. CH34. Extremophiles 4:77–82

    Article  CAS  PubMed  Google Scholar 

  • Niu X, Song L, Xiao Y, Ge W (2018) Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semi-arid agroecosystem and their potential in alleviating drought stress. Front Microbiol 8:2580

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Brien S, Hodgson DJ, Buckling A (2014) Social evolution of toxic metal bioremediation in Pseudomonas aeruginosa. Proc R Soc B Biol Sci 281(1787):20140858

    Article  Google Scholar 

  • Orcutt KM, Jones WS, McDonald A, Schrock D, Wallace KJ (2010) A lanthanide-based chemosensor for bioavailable Fe3+ using a fluorescent siderophore: an assay displacement approach. Sensors 10(2):1326–1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pande A, Pandey P, Mehra S et al (2017) Phenotypic and genotypic characterization of phosphate solubilizing bacteria and their efficiency on the growth of maize. J Genet Eng Biotechnol 15:379–391

    Article  PubMed  PubMed Central  Google Scholar 

  • Paul D, Sinha SN (2017) Isolation and characterization of phosphate solubilizing bacterium Pseudomonas aeruginosa KUPSB12 with antibacterial potential from river Ganga, India. Ann Agrar Sci 15:130–136

    Article  Google Scholar 

  • Payne SM (1993) Iron acquisition in microbial pathogenesis. Trends Microbiol 1:66–69

    Article  CAS  PubMed  Google Scholar 

  • Peek ME, Bhatnagar A, McCarty NA, Zughaier SM (2012) Pyoverdine, the major siderophore in Pseudomonas aeruginosa, evades NGAL recognition. Interdiscip Perspect Infect Dis 2012:843509

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira SIA, Castro PML (2014) Diversity and characterization of culturable bacterial endophytes from Zea mays and their potential as plant growth-promoting agents in metal-degraded soils. Environ Sci Pollut Res 21:14110–14123

    Article  CAS  Google Scholar 

  • Płociniczak T, Chodór M, Pacwa-Płociniczak M, Piotrowska-Seget Z (2019) Metal-tolerant endophytic bacteria associated with Silene vulgaris support the Cd and Zn phytoextraction in non-host plants. Chemosphere 219:250–260

    Article  PubMed  Google Scholar 

  • Rajkumar M, Freitas H (2008) Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Bioresour Technol 99:3491–3498

    Article  CAS  PubMed  Google Scholar 

  • Rajkumar M, Ae N, Freitas H (2010) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160

    Article  Google Scholar 

  • Rangan P, Subramani R, Kumar R et al (2014) Recent advances in polyamine metabolism and abiotic stress tolerance. Biomed Res Int 2014:239621

    Article  PubMed  PubMed Central  Google Scholar 

  • Rathi MS, Paul S, Thakur JK (2014) Response of wheat to inoculation with mycorrhizae alone and combined with selected rhizobacteria including Flavobacterium sp. as a potential bioinoculant. J Plant Nutr 37:76–86

    Article  CAS  Google Scholar 

  • Rathnayake IVN, Megharaj M, Krishnamurti GSR et al (2013) Heavy metal toxicity to bacteria—are the existing growth media accurate enough to determine heavy metal toxicity? Chemosphere 90:1195–1200

    Article  CAS  PubMed  Google Scholar 

  • Reis RS, de Moura VE, Heringer AS et al (2016) Putrescine induces somatic embryo development and proteomic changes in embryogenic callus of sugarcane. J Proteomics 130:170–179

    Article  CAS  PubMed  Google Scholar 

  • Retamal-Morales G, Mehnert M, Schwabe R et al (2018) Detection of arsenic-binding siderophores in arsenic-tolerating Actinobacteria by a modified CAS assay. Ecotoxicol Environ Saf 157:176–181

    Article  CAS  PubMed  Google Scholar 

  • Román-Ponce B, Ramos-Garza J, Arroyo-Herrera I et al (2018) Mechanism of arsenic resistance in endophytic bacteria isolated from endemic plant of mine tailings and their arsenophore production. Arch Microbiol 200:883–895

    Article  PubMed  Google Scholar 

  • Roy S, Roy M (2019) Characterization of plant growth promoting feature of a neutromesophilic, facultatively chemolithoautotrophic, sulphur oxidizing bacterium Delftia sp. strain SR4 isolated from coal mine spoil. Int J Phytoremediat 21:531–540

    Article  CAS  Google Scholar 

  • Roy S, Khasa DP, Greer CW (2007) Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contaminated ecosystems. Botany 85:237–251

    CAS  Google Scholar 

  • Saha M, Sarkar S, Sarkar B et al (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res 23:3984–3999

    Article  CAS  Google Scholar 

  • Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:30

    Google Scholar 

  • Sarkar A, Kazy SK, Sar P (2013) Characterization of arsenic resistant bacteria from arsenic rich groundwater of West Bengal, India. Ecotoxicology 22:363–376

    Article  CAS  PubMed  Google Scholar 

  • Sarwar N, Malhi SS, Zia MH et al (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937

    Article  CAS  PubMed  Google Scholar 

  • Schenkeveld WDC, Oburger E, Gruber B et al (2014) Metal mobilization from soils by phytosiderophores—experiment and equilibrium modeling. Plant Soil 383:59–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scherf U, Ross DT, Waltham M et al (2000) A gene expression database for the molecular pharmacology of cancer. Nat Genet 24:236

    Article  CAS  PubMed  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  • Silva Filho GN, Vidor C (2000) Solubilização de fostatos por microrganismos na presença de fontes de carbono. Rev Bras Ciência Do Solo 24:311–319

    Article  CAS  Google Scholar 

  • Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:599–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava S, Verma PC, Chaudhry V et al (2013) Influence of inoculation of arsenic-resistant Staphylococcus arlettae on growth and arsenic uptake in Brassica juncea (L.) Czern. Var. R-46. J Hazard Mater 262:1039–1047

    Article  CAS  PubMed  Google Scholar 

  • Sulaymon AH, Abdulmajeed BA, Salman AB (2015) Electrochemical removal of cadmium from simulated wastewater using a smooth rotating cylinder electrode. Desalin Water Treat 54:2557–2563

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N et al (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tank N, Saraf M (2009) Enhancement of plant growth and decontamination of nickel-spiked soil using PGPR. J Basic Microbiol 49:195–204

    Article  CAS  PubMed  Google Scholar 

  • Taurian T, Anzuay MS, Angelini JG et al (2010) Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant Soil 329:421–431

  • Thatoi H, Das S, Mishra J et al (2014) Bacterial chromate reductase, a potential enzyme for bioremediation of hexavalent chromium: a review. J Environ Manage 146:383–399

    Article  CAS  PubMed  Google Scholar 

  • Thieken A, Winkelmann G (1992) Rhizoferrin: a complexone type siderophore of the mocorales and entomophthorales (Zygomycetes). FEMS Microbiol Lett 94:37–41

    Article  CAS  Google Scholar 

  • Tiwari S, Lata C (2018) Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Front Plant Sci 9:452

    Article  PubMed  PubMed Central  Google Scholar 

  • Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117

    Article  CAS  PubMed  Google Scholar 

  • Tiwari S, Prasad V, Chauhan PS, Lata C (2017) Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Front Plant Sci 8:1510

    Article  PubMed  PubMed Central  Google Scholar 

  • Torres Z, Mora MA, Taylor RJ, Alvarez-Bernal D (2016) Tracking metal pollution in lake chapala: concentrations in water, sediments, and fish. Bull Environ Contam Toxicol 97:418–424. https://doi.org/10.1007/s00128-016-1892-6

    Article  CAS  PubMed  Google Scholar 

  • Trujillo-Cárdenas JL, Saucedo-Torres NP, Zárate del Valle PF et al (2010) Speciation and sources of toxic metals in sediments of Lake Chapala, Mexico. J Mex Chem Soc 54:79–87

    Google Scholar 

  • Vejan P, Abdullah R, Khadiran T et al (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21:573

    Article  PubMed Central  Google Scholar 

  • Volesky B (2001) Detoxification of metal-bearing effluents: biosorption for the next century. Hydrometallurgy 59:203–216

    Article  CAS  Google Scholar 

  • Vuosku J, Suorsa M, Ruottinen M et al (2012) Polyamine metabolism during exponential growth transition in Scots pine embryogenic cell culture. Tree Physiol 32:1274–1287

    Article  CAS  PubMed  Google Scholar 

  • Vuosku J, Karppinen K, Muilu-Mäkelä R et al (2018) Scots pine aminopropyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants. Ann Bot 121:1243–1256

  • Wilson MK, Abergel RJ, Raymond KN et al (2006) Siderophores of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. Biochem Biophys Res Commun 348:320–325

    Article  CAS  PubMed  Google Scholar 

  • Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379

    Article  CAS  PubMed  Google Scholar 

  • Wu W, Huang H, Ling Z et al (2016) Genome sequencing reveals mechanisms for heavy metal resistance and polycyclic aromatic hydrocarbon degradation in Delftia lacustris strain LZ-C. Ecotoxicology 25:234–247

    Article  CAS  PubMed  Google Scholar 

  • Wu Z, Kong Z, Lu S et al (2019) Isolation, characterization and the effect of indigenous heavy metal-resistant plant growth-promoting bacteria on sorghum grown in acid mine drainage polluted soils. J Gen Appl Microbiol 65(5):254–264

    Article  CAS  PubMed  Google Scholar 

  • Xu D, Guo J, Xu L et al (2014) The relationship between polyamine oxidase activity and lignin deposition and chrysanthemum flower bud differentiation. Acta Agric Boreali Sin 29:164–169

    Google Scholar 

  • Yadav M, Gupta R & Sharma RK (2019) Green and sustainable pathways for wastewater purification. In: Advances in water purification techniques, Elsevier, pp 355–383

  • Yokobe T, Hyodo F, Tokuchi N (2018) Seasonal effects on microbial community structure and nitrogen dynamics in temperate forest soil. Forests 9:153

    Article  Google Scholar 

  • Zahid M (2015) Isolation and identification of indigenous plant growth promoting rhizobacteria from Himalayan region of Kashmir and their effect on improving growth and nutrient contents of maize (Zea mays L.). Front Microbiol 6:207

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaidi A, Khan M, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hung 56:263–284

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, He L, Chen Z et al (2011) Characterization of ACC deaminase-producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere 83:57–62

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Huang Z, He L, Sheng X (2012) Assessment of bacterial communities and characterization of lead-resistant bacteria in the rhizosphere soils of metal-tolerant Chenopodium ambrosioides grown on lead–zinc mine tailings. Chemosphere 87:1171–1178

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was financially supported by the projects SIP20140353, SIP20140354, SIP20150311 and SIP20150358. J Maldonado-Hernández, I. Arroyo-Herrera and J. Guevara-Luna received scholarships from the Consejo Nacional de Ciencia y Tecnología (CONACyT) and BEIFI-IPN. B. Román-Ponce appreciates the support of Sistema Nacional de Investigadores-CONACyT. P. Estrada-de los Santos, E. T. Wang and M. S. Vásquez-Murrieta appreciate the scholarships of Comisión de Operación y Fomento de Actividades Académicas-IPN and Estímulos al Desempeño de los Investigadores-IPN and Sistema Nacional de Investigadores-CONACyT.

Funding

This study was financially supported by the projects: “Instituto Politécnico Nacional (IPN)” SIP20140353, SIP20140354, SIP20150311 and SIP20150358. J.M.H., I. A. H., J. G. L. received grant-aided support from “Consejo Nacional de Ciencia y Tecnología (CONACyT)” and BEIFI-IPN. P. E. S., E. T. W. and M. S. V. M. received grant-aided support from “Comisión de Operación y Fomento de Actividades Académicas-IPN” and “Estímulos al Desempeño de los Investigadores-IPN” and “Sistema Nacional de Investigadores (SNI)-CONACyT”. B.R. P. received grant-aided support from SIN-CONACyT. We thank Dra. Dioselina Álvarez-Bernal for access and guidance in soil sampling.

Author information

Author notes

  1. Jessica Maldonado-Hernández and Brenda Román-Ponce contributed equally to this work.

Authors and Affiliations

  1. Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, Prolongación Carpio y Plan de Ayala S/N, Col. Santo Tomás, Alcaldía Miguel Hidalgo, C.P. 11340, Mexico City, Mexico

    Jessica Maldonado-Hernández, Ivan Arroyo-Herrera, Joseph Guevara-Luna, Paulina Estrada de los Santos, En Tao Wang & María Soledad Vásquez-Murrieta

  2. Universidad Politécnica del Estado de Morelos, Boulevard Cuauhnáhuac 556, Lomas del Texcal, 62550, Jiutepec, Morelos, Mexico

    Brenda Román-Ponce

  3. Universidad del Valle de México, Campus Chapultepec, Laboratorio 314, Observatorio No. 400, Col. 16 de Septiembre, Del. Miguel Hidalgo, C.P. 11810, Mexico City, Mexico

    Jessica Maldonado-Hernández & Juan Ramos-Garza

  4. Instituto Mexicano del Petróleo, Eje Central Lázaro Cárdenas 152, Col. San Bartolo Atepehuacan, 07730, Mexico City, Mexico

    Salvador Embarcadero-Jiménez

Authors
  1. Jessica Maldonado-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brenda Román-Ponce
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ivan Arroyo-Herrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joseph Guevara-Luna
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juan Ramos-Garza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Salvador Embarcadero-Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paulina Estrada de los Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. En Tao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. María Soledad Vásquez-Murrieta
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JMH, BRP, JRG, PES, EW and MSVM were involved in the design of the project. JMH, BRP and JRG standardized the methodology. JMH, IAH, and BRP evaluate the metallophore production and PGP characteristics. BRP, JGL and SEJ analyzed the obtained data. BRP, PES, EW and MSVM wrote the manuscript. All the authors read and approved the final manuscript. MSVM supervised each stage of the experiment.

Corresponding author

Correspondence to María Soledad Vásquez-Murrieta.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maldonado-Hernández, J., Román-Ponce, B., Arroyo-Herrera, I. et al. Metallophores production by bacteria isolated from heavy metal-contaminated soil and sediment at Lerma–Chapala Basin. Arch Microbiol 204, 180 (2022). https://doi.org/10.1007/s00203-022-02780-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-022-02780-6

Keywords

Search

Navigation