Skip to main content

Bacterial Siderophore-Mediated Iron Acquisition in Cuatro Cienegas Basin: A Complex Community Interplay Made Simpler in the Light of Evolutionary Genomics

  • Chapter
  • First Online:
Ecosystem Ecology and Geochemistry of Cuatro Cienegas

Abstract

Ferric iron (Fe3+) became abundant after the oxidation event that occurred during the Precambrian, but biologically limited due to its poor and uneven distribution in its soluble form, ferrous iron (Fe2+). In consequence, siderophores, i.e., specialized iron scavenger metabolites, evolved to allow bacteria to obtain this nutrient. Therefore, siderophores can mediate complex bacterial communities, emphasizing the ecological role of these specialized metabolites. In this chapter, we present what is known about hydroxamate siderophores and, in particular, about coelichelin and desferrioxamines that are produced by genera belonging to the phylum Actinobacteria. Given that this phylum is predominant in Cuatro Cienegas Basin (CCB), our interest is in the evolution and ecological roles of these specialized metabolites in this unique ecological niche. We review the biosynthetic and transport capabilities sustaining bacterial hydroxamate siderophore-mediated iron acquisition in Actinobacteria and provide an example to illustrate a proposed evolutionary conceptual frameworkuseful for molecular functional and ecological analyses. The example presented includes genomic analysis of novel actinobacteria that were isolated from CCB that leads to novel biological insights, informing us about the structure and function of the microbial community as mediated by hydroxamate siderophores.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ahmed E, Holmström SJM (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7:196–208

    Article  CAS  Google Scholar 

  • Arias AA, Lambert S, Martinet L et al (2015) Growth of desferrioxamine deficient Streptomyces mutants through xenosiderophore piracy of airborne fungal contaminations. FEMS Microbiol Ecol 91:fiv080

    Article  Google Scholar 

  • Barona-Gómez F, Wong U, Giannakopulos AE et al (2004) Identification of a Cluster of Genes that Directs Desferrioxamine Biosynthesis in Streptomyces coelicolor M145. J Am Chem Soc 126:16282–16283

    Article  Google Scholar 

  • Barona-Gómez F, Lautru S, Francou FX, Leblond P, Pernodet JL, Challis GL et al (2006) Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877. Microbiology 152:3355–3366

    Article  Google Scholar 

  • Boiteau R, Mende D, Hawco N et al (2016) Siderophore-based adaptations to iron scarcity. PNAS 113:14237–14242

    Article  CAS  Google Scholar 

  • Boonlarppradab C (2007) Investigation of the potential anticancer and antifungal active secondary metabolites from marine natural products. Peer reviewed/Thesis/dissertation, UC San Diego

    Google Scholar 

  • Bruns H, Crüsemann M, Letzel A et al (2018) Function-related replacement of bacterial siderophore pathways. ISME J 12:320–329

    Article  CAS  Google Scholar 

  • Bunet R, Brock A, Rexer HU et al (2006) Identification of genes involved in siderophore transport in Streptomyces coelicolor A3(2). FEMS Microbiol Lett 262:57–64

    Article  CAS  Google Scholar 

  • Caspi A, Hariri AR, Holmes A et al (2010) Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am J Psychiatry 167:509–527

    Article  Google Scholar 

  • Challis G, Hopwood D (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. PNAS 100(Suppl 2):14555–14561

    Article  CAS  Google Scholar 

  • Cibrián-Jaramillo A, Barona-Gómez F (2016) Increasing metagenomic resolution of microbiome interactions through functional phylogenomics and bacterial sub-communities. Front Genet 10(7):4

    Google Scholar 

  • Codd R, Richardson-Sanchez T, Telfer TJ et al (2018) Advances in the chemical biology of Desferrioxamine B. ACS Chem Biol 13:11–25

    Article  CAS  Google Scholar 

  • Cornelis P, Andrews SC (2010) Iron uptake and homeostasis in microorganisms. Caister Academic Press, Norfolk

    Google Scholar 

  • Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F et al (2013) The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island. Genome Biol Evol 5:1165–1175

    Article  Google Scholar 

  • Cruz-Morales P, Ramos-Aboites HE, Licona-Cassani C et al (2017) Actinobacteria phylogenomics, selective isolation from an iron oligotrophic environment and siderophore functional characterization, unveil new desferrioxamine traits. FEMS Microbiol Ecol 93(9):fix086. https://doi.org/10.1093/femsec/fix086

    Article  CAS  PubMed Central  Google Scholar 

  • D’Onofrio A, Crawford JM, Stewart EJ et al (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17:254–264

    Article  Google Scholar 

  • Des Marais DL, Rausher MD (2008) Evidence for escape from adaptive conflict. Nature 454:762–765

    Article  Google Scholar 

  • Essen SA, Johnsson A, Bylund D et al (2007) Siderophore production by Pseudomonas stutzeri under aerobic and anaerobic conditions. Appl Environ Microbiol 73:5857–5864

    Article  CAS  Google Scholar 

  • Fardeau S, Mullié C, Dassonville-Klimpt A et al (2011) Bacterial iron uptake: a promising solution against multidrug resistant bacteria. In: Méndez-Vilas A (ed) Science against microbial pathogens: Communicating current research and technological advances. Formatex, Badajoz, pp 695–705

    Google Scholar 

  • Galet J, Deveau A, Hotel L et al (2015) Pseudomonas fluorescens pirates both ferrioxamine and ferricoelichelin siderophores from Streptomyces ambofaciens. Appl Environ Microbiol 81:3132–3141

    Article  CAS  Google Scholar 

  • Goswami D, Pithwa S, Dhandhukia P et al (2014) Delineating Kocuria turfanensis 2M4 as a credible PGPR: a novel IAA-producing bacterium isolated from saline desert. J Plant Interact 9:566–576

    Article  CAS  Google Scholar 

  • Gouda S, Kerry R, Das G et al (2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206:131–140

    Article  Google Scholar 

  • Gubbens J, Wu C, Zhu H et al (2017) intertwined precursor supply during biosynthesis of the catecholate-hydroxamate siderophores qinichelins in Streptomyces sp. MBT76. ACS Chem Biol 12:2756–2766

    Article  CAS  Google Scholar 

  • Guo X, Liu N, Li X et al (2015) Red soils harbor diverse culturable actinomycetes that are promising sources of novel secondary metabolites. Appl Environ Microbiol 81:3086–3103

    Article  CAS  Google Scholar 

  • Gutiérrez-García K, Neira-González A, Pérez-Gutiérrez R et al (2017) Phylogenomics of 2,4-Diacetylphloroglucinol-Producing Pseudomonas and Novel Antiglycation Endophytes from Piper auritum. J Nat Prod 80:1955–1963

    Article  Google Scholar 

  • Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27:637–657

    Article  CAS  Google Scholar 

  • Holden VI, Bachman MA (2015) Diverging roles of bacterial siderophores during infection. Metallomics 7:986–995

    Article  CAS  Google Scholar 

  • Hussain A, Rather M, Dar M et al (2018) Streptomyces puniceus strain AS13., Production, characterization and evaluation of bioactive metabolites: A new face of dinactin as an antitumor antibiotic. Microbiol Res 207:196–202

    Article  CAS  Google Scholar 

  • Kadi N, Oves-Costales D, Barona-Gómez F et al (2007) A new family of ATP-dependent oligomerization – macrocyclization biocatalysts. Nat Chem Biol 3:652–656

    Article  CAS  Google Scholar 

  • Kaur C, Kaur I, Raichand R et al (2011) Description of a novel actinobacterium Kocuria assamensis sp. nov., isolated from a water sample collected from the river Brahmaputra, Assam, India. Antonie Van Leeuwenhoek 99:721–726

    Article  CAS  Google Scholar 

  • Lambert S, Traxler MF, Craig M et al (2014) Altered desferrioxamine-mediated iron utilization is a common trait of bald mutants of Streptomyces coelicolor. Metallomics 6(8):1390–1399

    Article  CAS  Google Scholar 

  • Lautru S, Deeth RJ, Bailey LM et al (2005) Discovery of a new peptide natural product by Streptomyces coelicolor genome mining. Nat Chem Biol 1:265–269

    Article  CAS  Google Scholar 

  • Li D, Zheng W, Zhao J et al (2018) Lentzea soli sp. nov., an actinomycete isolated from soil. Int J Syst Evol Microbiol 68:1496–1501

    Article  Google Scholar 

  • Louden B, Haarmann D, Lynne AM (2011) Use of blue agar CAS assay for siderophore detection. J Microbiol Biol Educ 12:51–53

    Article  Google Scholar 

  • Messenger A, Barclay R (1983) Bacteria, iron and pathogenicity. Biochem Educ 11:54–63

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Monciardinni P, Iorio M, Maffioli S et al (2014) Discovering new bioactive molecules from microbial sources. Microb Biotechnol 7:209–220

    Article  Google Scholar 

  • Patel P, Song L, Challis GL (2010) Distinct extracytoplasmic siderophore binding proteins recognize ferrioxamines and ferricoelichelin in Streptomyces coelicolor A3(2). Biochemistry 49:8033–8042

    Article  CAS  Google Scholar 

  • Pessotti R, Hansen BL, Traxler MF (2018) In search of model ecological systems for understanding specialized metabolism. mSystems 3(2):e00175–e00117

    Article  Google Scholar 

  • Roberts AA, Schultz AW, Kersten RD et al (2012) Iron acquisition in the marine actinomycete genus Salinispora is controlled by the desferrioxamine family of siderophores. FEMS Microbiol Lett 335:95–103

    Article  CAS  Google Scholar 

  • Ronan J, Kadi N, McMahon S et al (2018) Desferrioxamine biosynthesis: diverse hydroxamate assembly by substrate-tolerant acyl transferase DesC. Philos Trans R Soc Lond B Biol Sci 373:20170068

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Senges C, Al-Dilaimi A, Marchbank D et al (2018) The secreted metabolome of Streptomyces chartreusis and implications for bacterial chemistry. PNAS 115:2490–2495

    Article  CAS  Google Scholar 

  • Smits TH, Duffy B (2011) Genomics of iron acquisition in the plant pathogen Erwinia amylovora insights in the biosynthetic pathway of the siderophore desferrioxamine E. Arch Microbiol 193:693–699

    Article  CAS  Google Scholar 

  • Souza V, Eguiarte L, Siefert J et al (2008) Microbial endemism: does phosphorus limitation enhance speciation? Nat Rev Microbiol 6(2008):559–564

    Article  CAS  Google Scholar 

  • Stackebrandt E, Koch C, Gvozdiak O et al (1995) Taxonomic dissection of the genus Micrococcus: Kocuria gen. nov., Nesterenkonia gen. nov., Kytococcus gen. nov., Dermacoccus gen. nov., and Micrococcus Cohn 1872 gen. emend. Int J Syst Bacteriol 45:682–692

    Article  CAS  Google Scholar 

  • Tierrafría VH, Ramos-Aboites HE, Gosset G et al (2011) Disruption of the siderophore-binding desE receptor gene in Streptomyces coelicolor A3(2) results in impaired growth in spite of multiple iron–siderophore transport systems. Microb Biotechnol 4:275–285

    Article  Google Scholar 

  • Traxler M, Kolter R (2015) Natural products in soil microbe interactions and evolution. Nat Prod Rep 32:956–970

    Article  CAS  Google Scholar 

  • Traxler MF, Seyedsayamdost MR, Clardy J et al (2012) Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 86:628–644

    Article  CAS  Google Scholar 

  • Traxler MF, Watrous JD, Alexandrov T et al (2013) Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. MBio 20:4

    Google Scholar 

  • Tunca S, Barreiro C, Sola-Landa A et al (2007) Transcriptional regulation of the desferrioxamine gene cluster of Streptomyces coelicolor is mediated by binding of DmdR1 to an iron box in the promoter of the desA gene. FEBS J 274:1110–1122

    Article  CAS  Google Scholar 

  • Tunca S, Barreiro C, Coque JJ et al (2009) Two overlapping antiparallel genes encoding the iron regulator DmdR1 and the Adm proteins control siderophore and antibiotic biosynthesis in Streptomyces coelicolor A3(2). FEBS J 276: 4814–4827

    Article  CAS  Google Scholar 

  • Wang W, Qiu Z, Tan H et al (2014) Siderophore production by actinobacteria. Biometals 27:623–631

    Article  CAS  Google Scholar 

  • Yamanaka K, Oikawa H, Ogawa HO et al (2005) Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis. Microbiology 151(Pt 9):2899–2905

    Article  CAS  Google Scholar 

  • Yassin AF, Rainey FA, Brzezinka H et al (1995) Lentzea gen. nov., a new genus of the order Actinomycetales. Int J Syst Bacteriol 45:357–363

    Article  CAS  Google Scholar 

  • Zhao P, Xue Y, Gao W et al (2018) Actinobacteria-Derived peptide antibiotics since 2000. Peptides 103:48–59

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The work by our laboratory in the CCB was made possible, thanks to the support by Valeria Souza and Gabriela Olmedo and their teams and funding to FBG from Conacyt grants (Nos. 179290 & 285746). The authors would like to thank the many members of the Evolution of Metabolic Diversity Laboratory that took part in expeditions to CCB during 2012–2016 and subsequent experimental and bioinformatics work. We would like to specially thank Alejandra Castañeda, Pablo Cruz, Milan Janda, Cuauhtémoc Licona, Paulina Mejía, Sandra Pérez, Hugo Ramírez, José-Luis Steffani, Nelly Selem, Karina Gutiérrez, and Mariana Vallejo, without whom this work could not have been possible.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Barona-Gómez .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ramos-Aboites, H., Yáñez-Olvera, A., Barona-Gómez, F. (2018). Bacterial Siderophore-Mediated Iron Acquisition in Cuatro Cienegas Basin: A Complex Community Interplay Made Simpler in the Light of Evolutionary Genomics. In: García-Oliva, F., Elser, J., Souza, V. (eds) Ecosystem Ecology and Geochemistry of Cuatro Cienegas. Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis. Springer, Cham. https://doi.org/10.1007/978-3-319-95855-2_10

Download citation

Publish with us

Policies and ethics