Skip to main content
SpringerLink
Log in

Formation of indigoidine derived-pigments contributes to the adaptation of Vogesella sp. strain EB to cold aquatic iron-oxidizing environments

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

We investigated previously under explored cold aquatic environments of Andean Patagonia, Argentina. Oily sheens similar to an oil spill are frequently observed at the surface of water in creeks and small ponds in these places. Chemical analysis of a water sample revealed the occurrence of high concentrations of iron and the presence of a free insoluble indigoidine-derived pigment. A blue pigment-producing bacterium (strain EB) was isolated from the water sample and identified as Vogesella sp. by molecular analysis. The isolate was able to produce indigoidine and another derived-pigment (here called cryoindigoidine) with strong antifreeze properties. The production of the pigments depended on the cell growth at cold temperatures (below 15 °C), as well as on the attachment of cells to solid surfaces, and iron limitation in the media. The pigments produced by strain EB showed an inhibitory effect on the growth of diverse microorganisms such as Candida albicans, Escherichia coli and Staphylococcus aureus. In addition, pigmented cells were more tolerant to freezing than non-pigmented cells, suggesting a role of cryoindigoidine/indigoidine as a cold-protectant molecule. The possible roles of the pigments in strain EB physiology and its interactions with the iron-rich environment from which the isolate was obtained are discussed. Results of this study suggested an active role of strain EB in the investigated iron-oxidizing ecosystem.

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
Fig. 7

Similar content being viewed by others

References

  • Alvarez HM, Silva RA, Cesari AC, Zamit AL, Peressutti SR, Reichelt R, Keller U, Malkus U, Rasch C, Maskow T, Mayer F, Steinbüchel A (2004) Physiological and morphological responses of the soil bacterium Rhodococcus opacus strain PD630 to water stress. FEMS Microbiol Ecol 50(2):75–86

    Article  CAS  PubMed  Google Scholar 

  • Andrews SC, Robinson AK, Rodriguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27(2–3):215–237

    Article  CAS  PubMed  Google Scholar 

  • Bequer Urbano S, Albarracín VH, Ordoñez OF, Farías ME, Alvarez HM (2013) Lipid storage in high-altitude Andean Lakes extremophiles and its mobilization under stress conditions in Rhodococcus sp. A5, a UV-resistant actinobacterium. Extremophiles 17(2):217–227

    Article  CAS  PubMed  Google Scholar 

  • Brachmann AO, Kirchner F, Kegler C, Kinski SC, Schmitt I, Bode HB (2012) Triggering the production of the cryptic blue pigment indigoidine from Photorhabdus luminescens. J Biotechnol 157(1):96–99

    Article  CAS  PubMed  Google Scholar 

  • Brandão LR, Libkind D, Vaz AB, Espírito Santo LC, Moliné M, de García V, van Broock M, Rosa CA (2011) Yeasts from an oligotrophic lake in Patagonia (Argentina): diversity, distribution and synthesis of photoprotective compounds and extracellular enzymes. FEMS Microbiol Ecol 76(1):1–13

    Article  PubMed  Google Scholar 

  • Castillo UF, Browne L, Strobel G, Hess WM, Ezra S, Pacheco G, Ezra D (2007) Biologically active endophytic streptomycetes from Nothofagus spp. and other plants in Patagonia. Microb Ecol 53(1):12–19

    Article  PubMed  Google Scholar 

  • Chan CS, Fakra SC, Emerson D, Fleming EJ, Edwards KJ (2011) Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation. ISME J 5(4):717–727

    Article  CAS  PubMed  Google Scholar 

  • Chu MK, Lin LF, Twu CS, Lin RH, Lin YC, Hsu ST, Tzeng KC, Huang HC (2010) Unique features of Erwinia chrysanthemi (Dickeya dadantii) RA3B genes involved in the blue indigoidine production. Microbiol Res 165(6):483–495

    Article  CAS  PubMed  Google Scholar 

  • Cude WN, Mooney J, Tavanaei AA, Hadden MK, Frank AM, Gulvik CA, May AL, Buchan A (2012) Production of the antimicrobial secondary metabolite indigoidine contributes to competitive surface colonization by the marine roseobacter Phaeobacter sp. strain Y4I. Appl Environ Microbiol 78(14):4771–4780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duckworth OW, Holmström SJM, Peña J, Sposito G (2009) Biogeochemistry of iron oxidation in a circumneutral freshwater habitat. Chem Geol 260:149–158

    Article  CAS  Google Scholar 

  • Emerson D, Revsbech NP (1994) Investigation of an iron-oxidizing microbial mat community located near Aarthus, Denmark: field studies. Appl Environ Microbiol 60(11):4022–4031

    CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17(6):368–376

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Felsenstein, J. (1993) PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle

  • Finking R, Marahiel MA (2004) Biosynthesis of nonribosomal peptides. Annu Rev Microbiol 58:453–488

    Article  CAS  PubMed  Google Scholar 

  • Fujikawa H, Akimoto R (2011) New pigment produced by Pantoea agglomerans and its production characteristics at various temperatures. Appl Environ Microbiol 77(1):172–178

    Article  CAS  PubMed  Google Scholar 

  • Grimes DJ, Woese CR, MacDonell MT, Colwell RR (1997) Systematic study of the genus Vogesella gen. nov. and its type species, Vogesella indigofera comb. nov. Int J Syst Bacteriol 47(1):19–27

    Article  CAS  PubMed  Google Scholar 

  • Heumann W, Young D, Gottlich C (1968) Leucoindigoidine formation by an Arthrobacter species and its oxidation to indigoidine by other micro-organisms. Biochim Biophys Acta 156(2):429–431

    Article  CAS  PubMed  Google Scholar 

  • Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of anurans. Syst Zool 18:1–32

    Article  Google Scholar 

  • Kuhn R, Starr MP, Kuhn DA, Bauer H, Knackmuss HJ (1965) Indigoidine and other bacterial pigments related to 3,3′-BipyridyI. Archly fiir Mikrobiologie 51:71–84

    Article  CAS  Google Scholar 

  • Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437(7057):376–380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Müller M, Ausländer S, Ausländer D, Kemmer C, Fussenegger M (2012) A novel reporter system for bacterial and mammalian cells based on the non-ribosomal peptide indigoidine. Metab Eng 14(4):325–335

    Article  PubMed  Google Scholar 

  • Nigam JN, Gogoi BK, Bezbaruah RL (1998) Short communication: alcoholic fermentation by agar-immobilized yeast cells. World J Microbiol Biotechnol 14:457–459

    Article  CAS  Google Scholar 

  • Notredame C, Higgins DG, Heringa J (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302(1):205–217

    Article  CAS  PubMed  Google Scholar 

  • Novakova R, Odnogova Z, Kutas P, Feckova L, Kormanec J (2010) Identification and characterization of an indigoidine-like gene for a blue pigment biosynthesis in Streptomyces aureofaciens CCM 3239. Folia Microbiol 55(2):119–125

    Article  CAS  Google Scholar 

  • Reichert J, Sakaitani M, Walsh CT (1992) Characterization of EntF as a serine-activating enzyme. Protein Sci 1(4):549–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reverchon S, Rouanet C, Expert D, Nasser W (2002) Characterization of indigoidine biosynthetic genes in Erwinia chrysanthemi and role of this blue pigment in pathogenicity. J Bacteriol 184(3):654–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouanet C, Nasser W (2001) The PecM protein of the phytopathogenic bacterium Erwinia chrysanthemi, membrane topology and possible involvement in the efflux of the blue pigment indigoidine. J Mol Microbiol Biotechnol 3(2):309–318

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  • Sawayama M, Suzuki T, Hashimoto H, Kasai T, Furutani M, Miyata N, Kunoh H, Takada J (2011) Isolation of a Leptothrix strain, OUMS1, from ocherous deposits in groundwater. Curr Microbiol 63(2):173–180

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Allen HK, Klimowicz AK, Mlot C, Gross JA, Savengsuksa S, McEllin J, Clardy J, Ruess RW, Handelsman J (2010) Psychrotrophic strain of Janthinobacterium lividum from a cold Alaskan soil produces prodigiosin. DNA Cell Biol 29(9):533–5341

    Article  CAS  PubMed  Google Scholar 

  • Starr MP, Cosens G, Knackmuss HJ (1966) Formation of the blue pigment indigoidine by phytopathogenic Erwinia. Appl Microbiol 14(6):870–872

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Zhang X, Broderick M, Fein H (2003) Measurement of nitric oxide production in biological systems by using Griess reaction assay. Sensors 3:276–284

    Article  CAS  Google Scholar 

  • Takahashi H, Kumagai T, Kitani K, Mori M, Matoba Y, Sugiyama M (2007) Cloning and characterization of a Streptomyces single module type non-ribosomal peptide synthetase catalyzing a blue pigment synthesis. J Biol Chem 282(12):9073–9081

    Article  CAS  PubMed  Google Scholar 

  • Tognetti C, Moliné M, van Broock M, Libkind D (2013) Favored isolation and rapid identification of the astaxanthin-producing yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma) from environmental samples. J Basic Microbiol 53(9):766–772

    Article  CAS  PubMed  Google Scholar 

  • Weber KA, Pollock J, Cole KA, O’Connor SM, Achenbach LA, Coates JD (2006) Anaerobic nitrate-dependent iron (II) bio-oxidation by a novel, lithoautotrophic, betaproteobacterium, strain 2002. Appl Environ Microbiol 72(1):686–694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu D, Xu F, Valiente J, Wang S, Zhan J (2013) An indigoidine biosynthetic gene cluster from Streptomyces chromofuscus ATCC 49982 contains an unusual IndB homologue. J Ind Microbiol Biotechnol 40(1):159–168

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the technical assistance of Dr. Gerardo Burton (University of Buenos Aires, Argentina) for the chemical analyses of the pigments and their interpretations. We also acknowledge Dr. Miguel Harvey (University of Patagonia SJB, Argentina) for crystallization analyses and discussions, and to Dr. Jorge Jaramillo Cisterna (University Austral of Chile) for fruitful discussions about results of chemical analyses. This study was financially supported by the SCyT of the University of Patagonia San Juan Bosco, and Project PICT2012 Nro. 2031 (ANPCyT), Argentina. Arrúa Day P. was recipient of a doctoral scholarship from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina. Alvarez H.M is a career investigator of CONICET.

Author information

Authors and Affiliations

  1. Instituto de Biociencias de La Patagonia (INBIOP), Universidad Nacional de La Patagonia San Juan Bosco Y CONICET, Km 4-Ciudad Universitaria, 9000, Comodoro Rivadavia, Chubut, Argentina

    Paula Arrúa Day, María S. Villalba, O. Marisa Herrero & Héctor M. Alvarez

  2. Oil M&S, Av. Hipólito Yrigoyen 4250, 9000, Comodoro Rivadavia, Chubut, Argentina

    María S. Villalba & O. Marisa Herrero

  3. Departamentode Química Orgánica, Facultad de Ciencias Naturales, Universidad Nacional de La Patagonia San Juan Bosco, Km 4-Ciudad Universitaria, 9000, Comodoro Rivadavia, Chubut, Argentina

    Luz Alejandra Arancibia

Authors
  1. Paula Arrúa Day
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María S. Villalba
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. Marisa Herrero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luz Alejandra Arancibia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Héctor M. Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Héctor M. Alvarez.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2460 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Day, P.A., Villalba, M.S., Herrero, O.M. et al. Formation of indigoidine derived-pigments contributes to the adaptation of Vogesella sp. strain EB to cold aquatic iron-oxidizing environments. Antonie van Leeuwenhoek 110, 415–428 (2017). https://doi.org/10.1007/s10482-016-0814-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-016-0814-2

Keywords

Search

Navigation