Skip to main content
Log in

Bioprospecting the potential of the microbial community associated to Antarctic marine sediments for hydrocarbon bioremediation

  • Environmental Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Microorganisms that inhabit the cold Antarctic environment can produce ligninolytic enzymes potentially useful in bioremediation. Our study focused on characterizing Antarctic bacteria and fungi from marine sediment samples of King George and Deception Islands, maritime Antarctica, potentially affected by hydrocarbon influence, able to produce enzymes for use in bioremediation processes in environments impacted with petroleum derivatives. A total of 168 microorganism isolates were obtained: 56 from sediments of King George Island and 112 from Deception Island. Among them, five bacterial isolates were tolerant to cell growth in the presence of diesel oil and gasoline and seven fungal were able to discolor RBBR dye. In addition, 16 isolates (15 bacterial and one fungal) displayed enzymatic emulsifying activities. Two isolates were characterized taxonomically by showing better biotechnological results. Psychrobacter sp. BAD17 and Cladosporium sp. FAR18 showed pyrene tolerance (cell growth of 0.03 g mL−1 and 0.2 g mL−1) and laccase enzymatic activity (0.006 UL−1 and 0.10 UL−1), respectively. Our results indicate that bacteria and fungi living in sediments under potential effect of hydrocarbon pollution may represent a promising alternative to bioremediate cold environments contaminated with polluting compounds derived from petroleum such as polycyclic aromatic hydrocarbons and dyes.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  1. Jurelevicius D, Cotta SR, Peixoto R, Rosado AS, Seldin L (2012) Distribution of alkane-degrading bacterial communities in soils from King George Island, Maritime Antarctic. Eur J Soil Biol 51:37–44

    Article  CAS  Google Scholar 

  2. Centurion VB, Silva JB, Duarte AWF, Rosa LH, Oliveira VM (2022) Comparing resistome profiles from anthropogenically impacted and non-impacted areas of two South Shetland Islands–Maritime Antarctica. Environ Pollut 304:119219

    Article  CAS  PubMed  Google Scholar 

  3. Ibrahim S et al (2020) Biosurfactant production and growth kinetics studies of the waste canola oil-degrading bacterium Rhodococcus erythropolis AQ5–07 from Antarctica. Molecules. https://doi.org/10.3390/molecules25173878

  4. Jesus HE, Peixoto RS, Rosado AS (2015) Bioremediation in Antarctic Soils. J Pet Environ Biotechnol. https://doi.org/10.4172/2157-7463.1000248

  5. Martins CDC, Bícego MC, Taniguchi S, Montone RC (2004) Aliphatic and polycyclic aromatic hydrocarbons in surface sediments in Admiralty Bay, King George Island, Antarctica. Antarctic Science 16(2):117–122

    Article  ADS  Google Scholar 

  6. Cripps GC, Shears J (1997) The fate in the marine environment of a minor diesel fuel spill from an Antarctic research station. Environ Monit Assess 46(3):221–232

    Article  CAS  Google Scholar 

  7. Duarte B et al (2021) First screening of biocides, persistent organic pollutants, pharmaceutical and personal care products in Antarctic phytoplankton from Deception Island by FT-ICR-MS. Chemosphere. https://doi.org/10.1016/j.chemosphere.2021.129860

  8. Moreira ER, Ottoni JR, De Oliveira VM, Passarini MRZ (2022) Potential for resistance to freezing by non-virulent bacteria isolated from Antarctica. An Acad Bras Ciênc. https://doi.org/10.1590/0001-3765202220210459

  9. Gran-Scheuch A, Ramos-Zuñiga J, Fuentes E, Bravo D, Pérez-Donoso JM (2020) Effect of co-contamination by PAHs and heavy metals on bacterial communities of diesel contaminated soils of South Shetland Islands, Antarctica. Microrganisms. https://doi.org/10.3390/microorganisms8111749

  10. Passarini MR, Rodrigues MV, da Silva M, Sette LD (2011) Marine-derived filamentous fungi and their potential application for polycyclic aromatic hydrocarbon bioremediation. Mar Pollut Bull 62:364–370

    Article  CAS  PubMed  Google Scholar 

  11. Krucon T, Dziewit L, Drewniak L (2021) Insight into ecology, metabolic potential, and the taxonomic composition of bacterial communities in the periodic water pond on King George Island (Antarctica). Front Microbiol. https://doi.org/10.3389/fmicb.2021.708607

  12. Passarini MRZ, Bernal SPF, Cecchet NL, Sartoratto A, Boroski M, Duarte AWF, Ottoni JR, Rosa LH, Oliveira VM (2020) Undecane production by cold-adapted bacteria from Antarctica. Extremophiles 24:863–873

    Article  CAS  PubMed  Google Scholar 

  13. Kita DM, Giovanella P, Yoshinaga TT, Pellizzer EP, Sette LD (2022) Antarctic fungi applied to textile dye bioremediation. An Acad Bras Cienc. https://doi.org/10.1590/0001-3765202220210234

  14. Trudgeon B, Dieser M, Balasubramanian N, Messmer M, Foreman CM (2020) Low-temperature biosurfactants from polar microbes. Microrganisms. https://doi.org/10.3390/microorganisms8081183

  15. Schultz J et al (2022) Polyphasic analysis reveals potential petroleum hydrocarbon degradation and biosurfactant production by rare biosphere thermophilic bacteria from Deception Island, an Active Antarctic Volcano. Front Microbiol. https://doi.org/10.3389/fmicb.2022.885557

  16. Benegas GRS, Bernal SPF, de Oliveira VM, Passarini MRZ (2021) Antimicrobial activity against Microcystis aeruginosa and degradation of microcystin-LR by bacteria isolated from Antarctica. Environ Sci Pollut Res 28(37):52381–52391

    Article  CAS  Google Scholar 

  17. Duarte AWF et al (2017) Cold-adapted enzymes produced by fungi from terrestrial and marine Antarctic environments. Crit Rev Biotechnol. https://doi.org/10.1080/07388551.2017.1379468

  18. Ribeiro ID, Oliveira B, Rodrigues A, Sibov S, Vieira JD (2016) avaliação da capacidade de degradação de hidrocarbonetos e fenol por isolados bacterianos endofíticos de bambu. Enciclopédia Biosfera 13(23)

  19. Brown HL, van Vliet AH, Betts RP, Reuter M (2013) Tetrazolium reduction allows assessment of biofilm formation by Campylobacter jejuni in a food matrix model. J Appl Microbiol 115(5):1212–1221. https://doi.org/10.1111/jam.12316

    Article  CAS  PubMed  Google Scholar 

  20. Bernal SP, Lira M, Jean-Baptiste J, Garcia PE, Batista E, Ottoni JR, Passarini MR (2021) Biotechnological potential of microorganisms from textile effluent: isolation, enzymatic activity and dye discoloration. An Acad Bras Ciênc. https://doi.org/10.1590/0001-3765202120191581

    Article  PubMed  Google Scholar 

  21. Martinho V, dos Santos Lima LM, Barros CA, Ferrari VB, Passarini MRZ, Santos LA ... de Vasconcellos SP (2019) Enzymatic potential and biosurfactant production by endophytic fungi from mangrove forest in Southeastern Brazil. AMB Express 9(1):1–8

  22. Nogueira OMN, Salgueiro JLG, Francisco EA, Ottoni JR, Passarini MRZ (2021) Tolerância de microrganismos eucariotos ao herbicida glifosato. Semina: Ciências Biológicas e da Saúde 42(1):103–112

    Google Scholar 

  23. Buswell JA, Cai Y, Chang ST (1995) Effect of nutrient nitrogen and manganese on manganese peroxidase and laccase production by Lentinula (Lentinus) edodes. FEMS Microbiol Lett 128(1):81–87

    Article  CAS  Google Scholar 

  24. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. https://doi.org/10.1007/BF01731581

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  26. Ottoni JR, e Silva TR, de Oliveira VM, Passarini MRZ (2020) Characterization of amylase produced by cold-adapted bacteria from Antarctic samples. Biocatal Agric Biotechnol 23:101452

    Article  Google Scholar 

  27. Ahn Y et al (2019) Oligotrophic media compared with a tryptic soy agar or broth for the recovery of Burkholderia cepacia complex from different storage temperatures and culture conditions. J Microbiol Biotechnol. https://doi.org/10.4014/jmb.1906.06024

    Article  PubMed  PubMed Central  Google Scholar 

  28. Raad M et al (2021) A defined medium based on R2A for cultivation and exometabolite profiling of soil bactéria. BioRxiv. https://doi.org/10.1101/2021.05.23.445362

    Article  Google Scholar 

  29. Wentzel LCP et al (2019) Fungi from Admiralty Bay (King George Island, Antarctica) Soils and Marine Sediments. Microb Ecol 77:12–24

    Article  ADS  CAS  PubMed  Google Scholar 

  30. Silva TR, Duarte AW, Passarini MR, Ruiz ALT, Franco CH, Moraes CB, Oliveira VM (2018) Bacteria from Antarctic environments: diversity and detection of antimicrobial, antiproliferative, and antiparasitic activities. Polar Biol 41:1505–1519

    Article  Google Scholar 

  31. Vicente J, Celis M, Alonso A, Marquina D, Santos A (2021) Microbial communities present in hydrothermal sediments from Deception Island, Antarctica. Microrganisms. https://doi.org/10.3390/microorganisms9081631

  32. Ferrés I, Amarelle V, Noya F, Fabiano E (1965). Identification of Antarctic culturable bacteria able to produce diverse enzymes of potential biotechnological interest. 极地研究, 26(1-English), 71

  33. Chang Y et al (2016) Degradation of toxic compounds at low and medium temperature conditions using isolated fungus. Clean – Soil Air Water. https://doi.org/10.1002/clen.201500753

  34. Ferrari BC, Zhang C, Van Dorst J (2011) Recovering greater fungal diversity from pristine and diesel fuel contaminated sub-Antarctic soil through cultivation using both a high and a low nutrient media approach. Front Microbiol 2:217. https://doi.org/10.3389/fmicb.2011.00217

    Article  PubMed  PubMed Central  Google Scholar 

  35. Wong RR et al (2021) Diesel in Antarctica and a bibliometric study on its indigenous microorganisms as remediation agent. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph18041512

    Article  PubMed  PubMed Central  Google Scholar 

  36. Sandoval-Denis M, Gené J, Sutton DA, Wiederhold NP, Cano-Lira JF, Guarro J (2016) New species of Cladosporium associated with human and animal infections. Persoonia. https://doi.org/10.3767/003158516X691951

    Article  PubMed  PubMed Central  Google Scholar 

  37. Rosa LH et al (2019) Fungi in Antarctica: diversity, ecology, effects of climate change, and bioprospection for bioactive compounds. In: Rosa L (eds) Fungi of Antarctica. Springer, Cham. pp 1–17. https://doi.org/10.1007/978-3-030-18367-7_1. Acessed 02 June 2022

  38. Kochkina G et al (2011) Ancient fungi in Antarctic permafrost environments. FEMS Microbiol Ecol 82:501–509

    Article  Google Scholar 

  39. Santos JA, Meyer E, Sette L D (2020) Fungal community in Antarctic soil along the retreating Collins Glacier (Fildes Peninsula, King George Island). Microrganisms. https://doi.org/10.3390/microorganisms8081145

  40. Newsham KK, Davey ML, Hopkins DW, Dennis PG (2021) Regional diversity of maritime Antarctic soil fungi and predicted responses of guilds and growth forms to climate change. Front Microbiol. https://doi.org/10.3389/fmicb.2020.615659

    Article  PubMed  PubMed Central  Google Scholar 

  41. Gunde-Cimerman N, Sonjak S, Zalar P, Frisvad JC, Diderichsen B, Plemenitaš A (2003) Extremophilic fungi in arctic ice: a relationship between adaptation to low temperature and water activity. Phys Chem Earth A/B/C 28(28–32):1273–1278

    Article  ADS  Google Scholar 

  42. Zalar PD, De Hoog GS, Schroers HJ, Crous PW, Groenewald JZ, Gunde-Cimerman N (2007) Phylogeny and ecology of the ubiquitous saprobe Cladosporium sphaerospermum, with descriptions of seven new species from hypersaline environments. Stud Mycol 58(1):157–183. https://doi.org/10.1038/s41598-020-78630-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Rosa LH et al (2020) DNA metabarcoding uncovers fungal diversity in soils of protected and non-protected areas on Deception Island, Antarctica. Sci Rep. https://doi.org/10.1038/s41598-020-78934-7

  44. Styczynski M et al (2022) Application of psychrotolerant antarctic bacteria and their metabolites as efficient plant growth promoting agents. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2022.772891

    Article  PubMed  PubMed Central  Google Scholar 

  45. Rizzo C et al (2020) Cultivable bacterial communities in brines from perennially ice-covered and pristine Antarctic Lakes: ecological and biotechnological implications. Microrganisms. https://doi.org/10.3390/microorganisms8060819

    Article  Google Scholar 

  46. Nóbrega F, Duarte RT, Torres-Ballesteros AM, Queiroz LL, Whyte LG, Pellizari VH (2021) Cold adapted desiccation-tolerant bacteria isolated from polar soils presenting high resistance to anhydrobiosis. bioRxiv

  47. Abdulrasheed M, Zakarua NN, Roslee AFA, Shukor MY, Zulkharnain A, Napis S, Convey P, Alias SA, Gonzalez-Rocha G, Ahmad SA (2020) Biodegradation of diesel oil by cold-adapted bacterial strains of Arthrobacter spp. from Antarctica. Antarctic Sci 32(5):341–353. https://doi.org/10.1017/S0954102020000206

    Article  ADS  Google Scholar 

  48. Panicker G, Aislabie J, Saul D, Bej AK (2002) Cold tolerance of Pseudomonas sp. 30–3 isolated from oil-contamined soil. Antarctica Polar Biol 25:5–11

    Article  Google Scholar 

  49. Gregson BH, Metodieva G, Metodiev MV, Golyshin PN, McKew BA (2020) Protein expression in the obligate hydrocarbon-degrading psychrophile Oleispira antarctica RB-8 during alkane degradation and cold tolerance. Environ Microbiol 22(5):1870–1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. de Jesus HE, Peixoto RS, Cury JC, van Elsas JD, Rosado AS (2015) Evaluation of soil bioremediation techniques in an aged diesel spill at the Antarctic Peninsula. Appl Microbiol Biotechnol 99:10815–10827

    Article  PubMed  Google Scholar 

  51. Zakaria NN, Convey P, Gomez-Fuentes C, Zulkharnain A, Sabri S, Shaharuddin NA, Ahmad SA (2021) Oil bioremediation in the marine environment of Antarctica: a review and bibliometric keyword cluster analysis. Microorganisms 9(2):419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. da Silva M, Passarini MRZ, Bonugli RC, Sette LD (2008) Cnidarian- derived filamentous fungi from Brazil: isolation characterization and RBBR decolourisation screening. Environ Technol 29

  53. Rovati JI, Pajot HF, Ruberto L, Cormack WM, Figueroa LIC (2013) Polyphenolic substrates and dyes degradation by yeasts from 25 de Mayo/King George Island (Antarctica). Yeast 30:459–470

    Article  CAS  PubMed  Google Scholar 

  54. Malavenda R et al (2015) Biosurfactant production by Arctic and Antarctic bacteria growing on hydrocarbons. Polar Biol 38:1565–1574

    Article  Google Scholar 

  55. Riccardi C et al (2022) Genome analysis of a new biosurfactants source: the Antarctic bacterium Psychrobacter sp. TAE2020. Mar Genomics. https://doi.org/10.1016/j.margen.2021.100922

  56. Coronel-León J, De Grau G, Grau-Campistany A, Farfan M, Rabanal F, Manresa A, Marqués AM (2015) Biosurfactant production by AL 1.1, a Bacillus licheniformis strain isolated from Antarctica: production, chemical characterization and properties. Ann Microbiol 65:2065–2078

    Article  Google Scholar 

  57. Bueno JDL, Santos PAD, da Silva RR, Moguel IS, Pessoa A Jr, Vianna MV, Gurpilhares DDB (2019) Biosurfactant production by yeasts from different types of soil of the South Shetland Islands (Maritime Antarctica). J Appl Microbiol 126(5):1402–1413

    Article  CAS  PubMed  Google Scholar 

  58. Gran-Scheuch A, Fuentes E, Bravo DM, Jiménez JC, Pérez-Donoso JM (2017) Isolation and characterization of phenanthrene degrading bacteria from diesel fuel-contaminated Antarctic soils. Front Microbiol

  59. Ausuri J, Vitale GA, Coppola D, Palma Esposito F, Buonocore C, de Pascale D (2021) Assessment of the degradation potential and genomic insights towards phenanthrene by Dietzia psychralcaliphila JI1D. Microorganisms 9(6):1327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Yumoto I et al (2002) Dietzia psychralcaliphila sp. nov., a novel, facultatively psychrophilic alkaliphile that grows on hydrocarbons. Int J Syst Evol Microbiol 52:85–90

    Article  CAS  PubMed  Google Scholar 

  61. Eriksson M, Dalhammar G, Mohn WW (2002) Bacterial growth and biofilm production on pyrene. FEMS Microbiol Ecol 40:21–27

    Article  CAS  PubMed  Google Scholar 

  62. Santos A, Burgos F, Martinez-Urtaza J, Barrientos L (2022) Metagenomic characterization of resistance genes in Deception Island and their association with mobile genetic elements. Microorganisms 10(7):1432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Martorell MM, Ruberto LAM, Castellanos LIF, Cormack WPM (2019) Bioremediation abilities of Antarctic fungi. In: Tiquia-Arashiro S, Grube M (eds) Fungi in extreme environments: ecological role and biotechnological significance. Springer, Cham. https://doi.org/10.1007/978-3-030-19030-9_26

    Chapter  Google Scholar 

  64. Govarthanan M, Fuzisawa S, Hosogai T, Chang Y (2017) Biodegradation of aliphatic and aromatic hydrocarbons using the filamentous fungus Penicillium sp. CHY-2 and characterization of its manganese peroxidase activity. RSC Adv 7:20716–20723

    Article  ADS  CAS  Google Scholar 

  65. Joshi-Navare K, Singh PK, Prabhune AA (2014) New yeast isolate Pichia caribbica synthesizes xylolipid biosurfactant with enhanced functionality. Eur J Lipid Sci Technol 116:1070–1079

    Article  CAS  Google Scholar 

  66. Hughes KA, Bridge P, Clark MS (2007) Tolerance of Antarctic soil fungi to hydrocarbons. Sci Total Environ 372:539–548

    Article  ADS  CAS  PubMed  Google Scholar 

  67. Silva MK et al (2022) Extracellular hydrolytic enzymes produced by yeasts from Antarctic lichens. An Acad Bras Cienc. https://doi.org/10.1590/0001-3765202220210540

  68. Duarte AWF et al (2018) Production of cold-adapted enzymes by flamentous fungi from King George Island, Antarctica. Polar Biol 41:2511–2521

    Article  Google Scholar 

  69. Yergeau E, Kowalchuk GA (2008) Responses of Antarctic soil microbial communities and associated functions to temperature and freeze–thaw cycle frequency. Environ Microbiol 10:2223–2235

    Article  PubMed  Google Scholar 

  70. Mukhopadhyay A, Dasgupta AK, Chakrabarti K (2015) Enhanced functionality and stabilization of a cold active laccase using nanotechnology based activation-immobilization. Bioresour Technol 179:573–584

    Article  CAS  PubMed  Google Scholar 

  71. Park HJ et al (2021) Involvement of laccase-like enzymes in humic substance degradation by diverse polar soil bactéria. Folia microbiol. https://doi.org/10.1007/s12223-020-00847-9

    Article  Google Scholar 

  72. Zhang A, Hou Y, Wang Q, Wang Y (2022) Characteristics and polyethylene biodegradation function of a novel cold-adapted bacterial laccase from Antarctic Sea Ice Psychrophile Psychrobacter Sp. Nj228. J Hazard Mater 439:129656

    Article  CAS  PubMed  Google Scholar 

  73. Préndez M, Barra C, Toledo C, Richter P (2011) Alkanes and polycyclic aromatic hydrocarbons in marine surficial sediment near Antarctic stations at Fildes Peninsula, King George Island. Antarctic Sci 23(6):578–588

    Article  ADS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Institutional Program Priority Latin America and the Caribbean EDITAL PRPPG No. 105/2020 and by the Program Institutional Triple Agenda EDITAL PRPPG No. 205/2021. CNPq PROANTAR 442258/2018-6, CAPES FAPEMI, and FNDCT

Author information

Authors and Affiliations

Authors

Contributions

LMC, MB, and MRZP carried out the analyses of the data; AWD, LHR, RV, and AAN collected the samples; AWD, VMO, and LHR reviewed the manuscript; JRO and MRZP wrote, reviewed, and edited the manuscript; all authors approved the final version of this manuscript.

Corresponding author

Correspondence to Michel R. Z. Passarini.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Luiz Henrique Rosa

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Melo Carlos, L., Camacho, K.F., Duarte, A.W. et al. Bioprospecting the potential of the microbial community associated to Antarctic marine sediments for hydrocarbon bioremediation. Braz J Microbiol 55, 471–485 (2024). https://doi.org/10.1007/s42770-023-01199-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-023-01199-5

Keywords

Navigation