Abstract
The resistance of microorganisms to heavy metals in polluted environments is mediated by genetically determined mechanisms. One such mechanism includes the intracellular sequestration of heavy metals in polyphosphate (polyP) inclusions. In Cr(III) contaminated mediums, Ochrobactrum anthropi DE2010 is able to bind and sequester Cr(III) in polyP inclusions. In order to further study the relationship between Cr(III) tolerance and polyP production in O. anthropi DE2010, we carried out whole genomic sequencing, analysis of single nucleotide polymorphisms (SNPs), polyP chemical quantification, and determination of the relative abundance and morphometry of polyP inclusions. In the O. anthropi DE2010 genome, six polyP and pyrophosphate (PPi) metabolic genes were found. Furthermore, genomic analysis via SNPs calling revealed that O. anthropi ATCC49188 and DE2010 strains had average variations of 1.51% in their whole genome sequences and 1.35% variation associated with the principal polyP metabolic gene cluster. In addition, the accumulation of polyP in the DE2010 strain and number of polyP inclusions found were directly correlated with the concentration of Cr(III) in contaminated cultures. The results presented in this study may enhance the understanding of polyP production in response to Cr(III) toxicity in the O. anthropi DE2010 strain. This knowledge may facilitate the successful removal of Cr(III) from the natural environment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acharya C, Apte SK (2013) Novel surface associated polyphosphate bodies sequester uranium in the filamentous, marine cyanobacterium, Anabaena torulosa. Metallomics 5(12):1595–1598
Andreeva N, Ryazanova L, Dmitriev V, Kulakovskaya T, Kulaev I (2014) Cytoplasmic inorganic polyphosphate participates in the heavy metal tolerance of Cryptococcus humicola. Folia Microbiol 59(5):381–389. https://doi.org/10.1007/s12223-014-0310-x
Akiyama M, Crooke E, Kornberg A (1993) An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. J Biol Chem 268(1):633–639
Albi T, Serrano A (2016) Inorganic polyphosphate in the microbial world. Emerging roles for a multifaceted biopolymer. World J Microbiol Biotechnol 32:27. https://doi.org/10.1007/s11274-015-1983-2
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91(7):869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075
Almeida MC, Branco R, Morais PV (2020) Response to vanadate exposure in Ochrobactrum tritici strains. PLoS ONE 15(2):e0229359. https://doi.org/10.1371/journal.pone.0229359
Alvarez S, Jerez CA (2004) Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans. Appl Environ Microbiol 70(9):5177–5182. https://doi.org/10.1128/AEM.70.9.5177-5182.2004
Anschutz P, Deborde J (2016) Spectrophotometric determination of phosphate in matrices from sequential leaching of sediments. Limnol Oceanogr Methods 14:245–256. https://doi.org/10.1002/lom3.10085
Aschar-Sobbi R, Abramov AY, Diao C, Kargacin ME, Kargacin JG, French JR, Pavlov E (2008) High sensitivity, quantitative measurements of polyphosphate using a new DAPI-based approach. J Fluoresc 18:859–866. https://doi.org/10.1007/s10895-008-0315-4
Aujoulat F, Romano-Bertrand S, Masnou A, Marchandin H, Jumas-Bilak E (2014) Niches, population structure and genome reduction in Ochrobactrum intermedium: clues to technology-driven emergence of pathogens. PLoS ONE 9(1):e83376. https://doi.org/10.1371/journal.pone.0083376
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021
Baratelli M, Maldonado J, Esteve I, Solé A, Diestra E (2010) Electron microscopy techniques and energy dispersive X-ray applied to determine the sorption of lead in Paracoccus sp. DE2007. In: Menendez-Vilas A (ed) Current research technology and education topics in applied microbiology and microbial biotechnology. Formatex Research Center, Badajoz, pp 1601–1608
Baxter M, Jensen TH (1980) Uptake of magnesium, strontium, barium, and manganese by Plectonema boryanum (Cyanophyceae) with special reference to polyphosphate bodies. Protoplasma 104:81–89
Boswell CD, Dick RE, Macaskie LE (1999) The effect of heavy metals and other environmental conditions on the anaerobic phosphate metabolism of Acinetobacter johnsonii. Microbiology 145(7):1711–1720. https://doi.org/10.1099/13500872-145-7-1711
Brown MR, Kornberg A (2004) Inorganic polyphosphate in the origin and survival of species. Proc Natl Acad Sci USA 101:16085–16087. https://doi.org/10.1073/pnas.0406909101
Burgos A, Maldonado J, De los Rios A, Solé A, Esteve I (2013) Effect of copper and lead on two consortia of phototrophic microorganisms and their capacity to sequester metals. Aquat Toxicol 140–141:324–336. https://doi.org/10.1016/j.aquatox.2013.06.022
Chain PSG, Lang DM, Comerci DJ, Malfatti SA, Vergez LM, Shin M, Ugalde RA, Garcia E, Tolmasky ME (2011) Genome of Ochrobactrum anthropi ATCC 49188T, a versatile opportunistic pathogen and symbiont of several eukaryotic hosts. J Bacteriol 193(16):4274–4275. https://doi.org/10.1128/JB.05335-11
Cheng Y, Yan F, Huang F, Chu W, Pan D, Chen Z, Zheng J, Yu M, Lin Z, Wu Z (2010) Bioremediation of Cr(VI) and immobilization as Cr(III) by Ochrobactrum anthropi. Environ Sci Technol 44(16):6357–6363. https://doi.org/10.1021/es100198v
Chojnacka K (2010) Biosorption and bioaccumulation—the prospects for practical applications. Environ Int 36:299–307
Choudhary S, Sar P (2011) Uranium biomineralization by a metal resistant Pseudomonas aeruginosa strain isolated from contaminated mine waste. J Hazard Mater 186(1):336–343. https://doi.org/10.1016/j.jhazmat.2010.11.004
Chourey K, Thompson MR, Morrell-Falvey J, VerBerkmoes NC, Brown SD, Shah M, Zhou J, Doktycz M, Hettich RL, Thompson DK (2006) Global molecular and morphological effects of 24-hour chromium(VI) exposure on Shewanella oneidensis MR-1. Appl Environ Microbiol 72:6331–6344
Diestra E, Esteve I, Burnat M, Maldonado J, Solé A (2007) Isolation and characterization of a heterotrophic bacterium able to grow in different environmental stress conditions, including crude oil and heavy metals. In: Méndez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology, FORMATEX
Eixler S, Selig U, Karsten U (2005) Extraction and detection methods for polyphosphate storage in autotrophic planktonic organisms. Hydrobiologia 533(1–3):135–143. https://doi.org/10.1007/s10750-004-2406-9
Fathima A, Rao JR (2018) Is Cr(III) toxic to bacteria: toxicity studies using Bacillus subtilis and Escherichia coli as model organism. Arch Microbiol 200:453–462. https://doi.org/10.1007/s00203-017-1444-4
Gerber U, Zirnstein I, Krawczyk-Bärsch E, Lünsdorf H, Arnold T, Merroun ML (2016) Combined use of flow cytometry and microscopy to study the interactions between the gram-negative betaproteobacterium Acidovorax facilis and uranium(VI). J Hazard Mater 317:127–134. https://doi.org/10.1016/j.jhazmat.2016.05.062
Gohil KN, Neurgaonkar PS, Paranjpe A, Dastager SG, Dharne MS (2016) Peeping into genomic architecture by re-sequencing of Ochrobactrum intermedium M86 strain during laboratory adapted conditions. Genomic Data 8:72–76. https://doi.org/10.1016/j.gdata.2016.04.003
Hansda A, Kumar V (2016) A comparative review towards potential of microbial cells for heavy metal removal with emphasis on biosorption and bioaccumulation. World J Microbiol Biotechnol 32:170. https://doi.org/10.1007/s11274-016-2117-1
Harold FM (1966) Inorganic polyphosphates in biology: structure, metabolism, and function. Bacteriol Rev 30:772–794
Jacobs JA, Testa SM (2005) Overview of chromium (VI) in the environment: background and history. In: Guertin J, Jacobs JA, Avakian CP (eds) Chromium (VI). Handbook CRC Press, Boca Raton, pp 1–22
Jensen TE, Rachlin JW, Jani V, Warkentine BE (1986) Heavy metal uptake in relation to phosphorus nutrition in Anabaena variabilis (Cyanophyceae). Environ Pollut 42(1986):261–271
Keasling JD, Bertsch L, Kornberg A (1993) Guanosine pentaphosphate phosphohydrolase of Escherichia coli is a long-chain exopolyphosphatase. Proc Natl Acad Sci USA 90(15):7029–7033. https://doi.org/10.1073/pnas.90.15.7029
Kornberg A, Rao NN, Ault-Riche D (1999) Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 68:89–125. https://doi.org/10.1016/j.str.2006.06.009
Kulakovskaya T (2018) Inorganic polyphosphates and heavy metal resistance in microorganisms. World J Microbiol Biotechnol 34:139. https://doi.org/10.1007/s11274-018-2523-7
Kulakovskaya T, Ryazanova L, Zvonarev A, Khokhlova G, Ostroumov V, Vainshtein M (2018) The biosorption of cadmium and cobalt and iron ions by yeast Cryptococcus humicola at nitrogen starvation. Folia Microbiol 63:507–510. https://doi.org/10.1007/s12223-018-0583-6
Kuroda A, Nomura K, Ohtomo R, Kato J, Ikeda T, Takiguchi N, Ohtake H, Kornberg A (2001) Role of inorganic polyphosphate in promoting ribosomal protein degradation by the ion protease in E. coli. Science 27:705–708. https://doi.org/10.1126/science.1061315
Lahti R, Pitkäranta T, Valve E, Ilta I, Kukko-Kalske E, Heinonen J (1988) Cloning and characterization of the gene encoding inorganic pyrophosphatase of Escherichia coli K-12. J Bacteriol 170(12):5901–5907
Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Lee HW, Park YK (2008) Characterizations of denitrifying polyphosphate-accumulating bacterium Paracoccus sp. strain YKP-9. J Microbiol Biotechnol 18(12):1958–1965. https://doi.org/10.4014/jmb.0800.162
Lee S, Lee Y, Lee Y, Choi Y (2006) Molecular characterization of polyphosphate (PolyP) operon from Serratia marcescens. J Basic Microbiol 46:108–115. https://doi.org/10.1002/jobm.200510038
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) 1000 Genome project data processing subgroup. The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Maldonado J, Diestra E, Domènech AM, Villagrasa E, Puyen ZM, Esteve I, Solé A (2010) Isolation and identification of a bacterium with high tolerance to lead and copper from a marine microbial mat in Spain. Ann Microbiol 60(1):113–120. https://doi.org/10.1007/s13213-010-0019-2
Masindi V, Muedi KL (2018) Environmental contamination by heavy metals. Heavy Metals, Hosam El-Din M. Saleh and Refaat F. Aglan, IntechOpen https://doi.org/10.5772/intechopen.76082
Millach L, Solé A, Esteve I (2015) Role of Geitlerinema sp. DE2011 and Scenedesmus sp. DE2009 as bioindicators and immobilizers of chromium in a contaminated natural environment. BioMed Res Int. https://doi.org/10.1155/2015/519769
Milloning G (1961) A modified procedure for lead staining of thin sections. J Biophys Biochem Cytol 11:736–739
Mukherjee C, Chowdhury R, Ray K (2015) Phosphorus recycling from an unexplored source by polyphosphate accumulating microalgae and Cyanobacteria-A step to phosphorus security in agriculture. Front Microbiol 6:1421. https://doi.org/10.3389/fmicb.2015.01421
Narancic T, Djokic L, Kenny ST, O’Connor KE, Radulovic V, Nikodinovic-Runic J, Vasiljevic B (2012) Metabolic versatility of Gram-positive microbial isolates from contaminated river sediments. J Hazard Mater 215–216:243–251. https://doi.org/10.1016/j.jhazmat.2012.02.059
Oehmen A, Carvalho G, Lopez-Vazquez CM, van Loosdrecht MCM, Reis MAM (2010) Incorporating microbial ecology into the metabolic modelling of polyphosphate accumulating organisms and glycogen accumulating organisms. Water Res 44(17):4992–5004. https://doi.org/10.1016/j.watres.2010.06.071
Oliveira H (2012) Chromium as an environmental pollutant: insights on induced plant toxicity. J Bot. https://doi.org/10.1155/2012/375843
Orell A, Navarro CA, Rivero M, Aguilar JS, Jerez CA (2012) Inorganic polyphosphates in extremophiles and their possible functions. Extremophiles 16:573. https://doi.org/10.1007/s00792-012-0457-9
Páez PL, Bazán CM, Bongiovanni ME, Toneatto J, Albesa I, Becerra MC, Argüello GA (2013) Oxidative stress and antimicrobial activity of chromium(III) and ruthenium(II) complexes on Staphylococcus aureus and Escherichia coli. BioMed Res Int. https://doi.org/10.1155/2013/906912
Plaper A, Jenko-Brinovec S, Premzl A, Kos J, Raspor P (2002) Genotoxicity of trivalent chromium in bacterial cells. Possible effects on DNA topology. Chem Res Toxicol 15:943–949. https://doi.org/10.1021/tx010096q
Puyen ZM, Villagrasa E, Maldonado J, Diestra E, Esteve I, Solé A (2012) Biosorption of lead and copper by heavy-metal tolerant Micrococcus luteus DE2008. Bioresour Technol 126:233–237. https://doi.org/10.1016/j.biortech.2012.09.036
Rao NN, Kornberg A (1996) Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J Bacteriol 178:1394–1400. https://doi.org/10.1128/jb.178.5.1394-1400.1996
Rao NN, Gomez-Garcia MR, Kornberg A (2009) Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78:60. https://doi.org/10.1146/annurev.biochem.77.083007.093039
Rea PA, Poole RJ (1993) Vacuolar H+-translocating pyrophosphatase. Annu Rev Plant Physiol Plant Mol Biol 44:157–180. https://doi.org/10.1042/bj0221446
Rubio-Rincón FJ, Lopez-Vazquez CM, Welles L, van Loosdrecht MCM, Brdjanovic D (2017) Cooperation between Candidatus Competibacter and Candidatus Accumulibacter clade I, in denitrification and phosphate removal processes. Water Res 120:156–164. https://doi.org/10.1016/j.watres.2017.05.001
Ruiz FA, Rodrigues CO, Docampo R (2001) Rapid changes in polyphosphate content within acidocalcisomes in response to cell growth, differentiation, and environmental stress in Trypanosoma cruzi. J Biol Chem 276:26114–26121. https://doi.org/10.1074/jbc.M102402200
Sayers EW, Agarwala R, Bolton EE, Brister JR, Canese K, Clark K, Connor R, Fiorini N, Funk K, Hefferon T, Holmes JB, Kim S, Kimchi A, Kitts PA, Lathrop S, Lu Z, Madden TL, Marchler-Bauer A, Phan L, Schneider VA, Schoch CL, Pruitt KD, Ostell J (2019) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 47:23–28. https://doi.org/10.1093/nar/gky1069
Sievers F, Higgins DG (2018) Clustal Omega for making accurate alignments of many protein sciences. Protein Sci 27:135–145. https://doi.org/10.1002/pro.3290
Suzuki Y, Banfield JF (2004) Resistance to, and accumulation of, uranium by bacteria from uranium-contaminated site. Geomicrobiol J 21:113–121
Villagrasa E, Ferrer-Miralles N, Millach L, Obiol A, Creus J, Esteve I, Sole A (2019) Morphological responses to nitrogen stress deficiency of a new heterotrophic isolated strain of Ebro Delta microbial mats. Protoplasma 256:105–116. https://doi.org/10.1007/s00709-018-1263-8
Villagrasa E, Ballesteros B, Olbiol A, Millach L, Esteve I, Sole A (2020) Multi-approach analysis to assess the chromium(III) immobilization by Ochrobactrum anthropi DE2010. Chemosphere 238:124663. https://doi.org/10.1016/j.chemosphere.2019.124663
Wilbur S, Abadin H, Fay M, Yu D, Tencza B, Ingerman L, Klotzbach J, James S (2012) Toxicological profile for chromium. Agency for Toxic Substances and Disease Registry (US), Atlanta
Zhang H, Ishige K, Kornberg A (2002) A polyphosphate kinase (PPK2) widely conserved in bacteria. Proc Natl Acad Sci USA 99:16678–16683. https://doi.org/10.1073/pnas.262655199
Acknowledgements
We express our thanks for CIBER in Bioengineering, Biomaterials & Nanomedicine (CIBER-BBN) financed by Instituto Carlos III with assistance from European Regional Development. The authors also acknowledge ICTS “NANBIOSIS”, and, more specifically, the Protein Production Platform of CIBER-BBN at the UAB sePBioES scientific-technical service (https://www.nanbiosis.es/portfolio/u1-protein-production-platform-ppp/) and to the UAB scientific-technical service SGB (https://sct.uab.cat/genomica-bioinformatica/es). We also appreciate the help and collaboration of Cristina Sosa, Estefania Solsona and Neus Bonet-Garcia and the valuable comments and suggestions of Prof. Isabel Esteve.
Funding
This research was supported by the following Grants of Ministerio de Economía y Competitividad (CTQ2014-54553-C3-2-R and CGL2008-01891 to AS and RTA2012-00028-C02-02 to NFM) and UAB postgraduate scholarship to EV.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest in this publication.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Villagrasa, E., Egea, R., Ferrer-Miralles, N. et al. Genomic and biotechnological insights on stress-linked polyphosphate production induced by chromium(III) in Ochrobactrum anthropi DE2010. World J Microbiol Biotechnol 36, 97 (2020). https://doi.org/10.1007/s11274-020-02875-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-020-02875-6