Skip to main content
Log in

Identification of a putatively multixenobiotic resistance related Abcb1 transporter in amphipod species endemic to the highly pristine Lake Baikal

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The fauna of Lake Baikal in Eastern Siberia, the largest freshwater body on Earth, is characterized by high degrees of biodiversity and endemism. Amphipods, a prominent taxon within the indigenous fauna, occur in an exceptionally high number of endemic species. Considering the specific water chemistry of Lake Baikal with extremely low levels of potentially toxic natural organic compounds, it seems conceivable that certain adaptions to adverse environmental factors are missing in endemic species, such as cellular defense mechanisms mitigating toxic effects of chemicals. The degree to which the endemic fauna is affected by the recently occurring anthropogenic water pollution of Lake Baikal may depend on the existence of such cellular defense mechanisms in those species. We here show that endemic amphipods express transcripts for Abcb1, a major component of the cellular multixenobiotic resistance (MXR) defense against toxic chemicals. Based on a partial abcb1 cDNA sequence from Gammarus lacustris, an amphipod species common across Northern Eurasia but only rarely found in Lake Baikal, respective homologous sequences were cloned from five amphipods endemic to Lake Baikal, Eulimnogammarus verrucosus, E. vittatus, E. cyaneus, E. marituji, and Gmelinoides fasciatus, confirming that abcb1 is transcribed in those species. The effects of thermal (25 °C) and chemical stress (1–2 mg L−1 phenanthrene) in short-term exposures (up to 24 h) on transcript levels of abcb1 and heat shock protein 70 (hsp70), used as a proxy for cellular stress in the experiments, were exemplarily examined in E. verrucosus, E. cyaneus, and Gammarus lacustris. Whereas increases of abcb1 transcripts upon treatments occurred only in the Baikalian species E. verrucosus and E. cyaneus but not in Gammarus lacustris, changes of hsp70 transcript levels were seen in all three species. At least for species endemic to Lake Baikal, the data thus indicate that regulation of the identified amphipod abcb1 is triggered within the general cellular stress response. This is the first report presenting molecular data on a MXR transporter in amphipods, an ecotoxicologically important but with regard to gene sequence data comparatively little explored taxon.

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
Fig. 5

Similar content being viewed by others

Notes

  1. Our designation of gene and protein names is abcb1/Abcb1 for amphipod and other invertebrates and ABCB1/ABCB1 for human (gene/protein).

References

  • Ambudkar SV, Kim IW, Sauna ZE (2006) The power of the pump: mechanisms of action of P-glycoprotein (ABCB1). Eur J Pharm Sci 27:392–400

    Article  CAS  Google Scholar 

  • Aquan-Yuen M, Mackay D, Shiu WY (1979) Solubility of hexane, phenanthrene, chlorobenzene and p-dichlorobenzene in aqueous electrolyte solutions. J Chem Eng Data 24:30–34

    Article  CAS  Google Scholar 

  • Bedulina DS, Evgen’ev MB, Timofeyev MA, Protopopova MV, Garbuz DG, Pavlichenko VV, Luckenbach T, Shatilina ZM, Axenov-Gribanov DV, Gurkov AN, Sokolova IM, Zatsepina OG (2013) Expression patterns and organization of the hsp70 genes correlate with thermotolerance in two congener endemic amphipod species (Eulimnogammarus cyaneus and E. verrucosus) from Lake Baikal. Mol Ecol 22:1416–1430

    Article  CAS  Google Scholar 

  • Berezina NA (2007) Invasions of alien amphipods (Amphipoda: Gammaridea) in aquatic ecosystems of North-Western Russia: pathways and consequences. Hydrobiologia 590:15–29

    Article  Google Scholar 

  • Bosch TCG, Krylow SM, Bode HR, Steele RE (1988) Thermotolerance and synthesis of heat-shock proteins - these responses are present in Hydra attenuata but absent in Hydra oligactis. Proc Natl Acad Sci U S A 85:7927–7931

    Article  CAS  Google Scholar 

  • Campos B, Altenburger R, Gomez C, Lacorte S, Pina B, Barata C, Luckenbach T (2014) First evidence for toxic defense based on the multixenobiotic resistance (MXR) mechanism in Daphnia magna. Aquat Toxicol 148C:139–151

    Article  Google Scholar 

  • Chen CJ, Chin JE, Ueda K, Clark DP, Pastan I, Gottesman MM, Roninson IB (1986) Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47:381–389

    Article  CAS  Google Scholar 

  • Dean M, Annilo T (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 6:123–142

    Article  CAS  Google Scholar 

  • Epel D (1998) Use of multidrug transporters as first lines of defense against toxins in aquatic organisms. Comp Biochem Phys A 120:23–28

    Article  Google Scholar 

  • Epel D, Luckenbach T, Stevenson CN, Macmanus-Spencer LA, Hamdoun A, Smital T (2008) Efflux transporters: newly appreciated roles in protection against pollutants. Environ Sci Technol 42:3914–3920

    Article  CAS  Google Scholar 

  • Eufemia NA, Epel D (2000) Induction of the multixenobiotic defense mechanism (MXR), P-glycoprotein, in the mussel Mytilus californianus as a general cellular response to environmental stresses. Aquat Toxicol 49:89–100

    Article  CAS  Google Scholar 

  • Eufemia N, Clerte S, Girshick S, Epel D (2002) Algal products as naturally occurring substrates for p-glycoprotein in Mytilus californianus. Mar Biol 140:343–353

    Article  CAS  Google Scholar 

  • Falkner KK, Measures CI, Herbelin SE, Edmond JM, Weiss RF (1991) The major and minor element geochemistry of Lake Baikal. Limnol Oceanogr 36:413–423

    Article  CAS  Google Scholar 

  • Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, Roth J, Hofmann AF, Meier PJ (1998) The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 273:10046–10050

    Article  CAS  Google Scholar 

  • Gladyshev MI, Moskvicheva AV (2002) Baikal invaders have become dominant in the upper Yenisei benthofauna. Dokl Biol Sci 383:138–140

    Article  CAS  Google Scholar 

  • Gökirmak T, Campanale JP, Shipp LE, Moy GW, Tao HC, Hamdoun A (2012) Localization and substrate selectivity of sea urchin multidrug (MDR) efflux transporters. J Biol Chem 287:43876–43883

    Article  Google Scholar 

  • Gray NK, Wickens M (1998) Control of translation initiation in animals. Annu Rev Cell Dev Bi 14:399–458

    Article  CAS  Google Scholar 

  • Gribar JJ, Ramachandra M, Hrycyna CA, Dey S, Ambudkar SV (2000) Functional characterization of glycosylation-deficient human P-glycoprotein using a vaccinia virus expression system. J Membrane Biol 173:203–214

    Article  CAS  Google Scholar 

  • Heumann J, Carmichael S, Bron JE, Tildesley A, Sturm A (2012) Molecular cloning and characterisation of a novel P-glycoprotein in the salmon louse Lepeophtheirus salmonis. Comp Biochem Phys C 155:198–205

    CAS  Google Scholar 

  • Hofmann GE (2005) Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45:247–255

    Article  CAS  Google Scholar 

  • Horio M, Gottesman MM, Pastan I (1988) ATP-dependent transport of vinblastine in vesicles from human multidrug-resistant cells. Proc Natl Acad Sci U S A 85:3580–3584

    Article  CAS  Google Scholar 

  • Ishibashi H, Iwata H, Kim EY, Tao L, Kannan K, Tanabe S, Batoev VB, Petrov EA (2008) Contamination and effects of perfluorochemicals in Baikal seal (Pusa sibirica). 2. Molecular characterization, expression level, and transcriptional activation of peroxisome proliferator-activated receptor alpha. Environ Sci Technol 42:2302–2308

    Article  CAS  Google Scholar 

  • Käll L, Krogh A, Sonnhammer ELL (2005) An HMM posterior decoder for sequence feature prediction that includes homology information. Bioinformatics 21:I251–I257

    Article  Google Scholar 

  • Karaman GS, Pinkster S (1977) Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda). Part I. Gammarus pulex-group and related species. Bijdragen Tot De Dierkunde 47:1–97

    Google Scholar 

  • Khozov M (1963) Lake Baikal and its life. Junk, The Hague

  • Kornfeld R, Kornfeld S (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54:631–664

    Article  CAS  Google Scholar 

  • Kozhova O, Izmest’eva L (1998) Lake Baikal - evolution and biodiversity. Backhuys, Leiden

    Google Scholar 

  • Kurelec B (1992) The multixenobiotic resistance mechanism in aquatic organisms. Crit Rev Toxicol 22:23–43

    Article  CAS  Google Scholar 

  • Luckenbach T, Epel D (2008) ABCB- and ABCC-type transporters confer multixenobiotic resistance and form an environment-tissue barrier in bivalve gills. Am J Physiol Regul Integr Comp Physiol 294:R1919–R1929

    Article  CAS  Google Scholar 

  • Mackay D, Shiu WY (1977) Aqueous solubility of polynuclear aromatic hydrocarbons. J Chem Eng Data 22:399–402

    Article  CAS  Google Scholar 

  • Miyazaki M, Kohno K, Uchiumi T, Tanimura H, Matsuo K, Nasu M, Kuwano M (1992) Activation of human multidrug resistance-1 gene promoter in response to heat shock stress. Biochem Biophys Res Commun 187:677–684

    Article  CAS  Google Scholar 

  • Muller M, Yong M, Peng XH, Petre B, Arora S, Ambudkar SV (2002) Evidence for the role of glycosylation in accessibility of the extracellular domains of human MRP1 (ABCC1). Biochemistry 41:10123–10132

    Article  Google Scholar 

  • Nakano K, Iwama GK (2002) The 70-kDa heat shock protein response in two intertidal sculpins, Oligocottus maculosus and O. snyderi: relationship of hsp70 and thermal tolerance. Comp Biochem Phys A 133:79–94

    Article  Google Scholar 

  • Nota B, Bosse M, Ylstra B, van Straalen NM, Roelofs D (2009) Transcriptomics reveals extensive inducible biotransformation in the soil-dwelling invertebrate Folsomia candida exposed to phenanthrene. BMC Genomics 10:236

    Article  Google Scholar 

  • Parsell DA, Lindquist S (1994) Heat shock proteins and stress tolerance. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor, Plainview, pp 457–494

    Google Scholar 

  • Pfaffl MW (2004) Quantification strategies in real-time PCR. In: Bustin S (ed) A-Z of quantitative PCR. International University Line (IUL), La Jolla, pp 87–112

    Google Scholar 

  • Pfaffl MW (2006) Relative quantification. In: Dorak MT (ed) Real-time PCR. Taylor & Francis Group, New York, pp 63–82

    Google Scholar 

  • Protopopova MV, Pavlichenko VV, Menzel R, Putschew A, Luckenbach T, Steinberg CE (2014) Contrasting cellular stress responses of Baikalian and Palearctic amphipods upon exposure to humic substances: environmental implications. Environ Sci Pollut Res Int. doi:10.1007/s11356-014-3323-8

  • Scotto KW (2003) Transcriptional regulation of ABC drug transporters. Oncogene 22:7496–7511

    Article  CAS  Google Scholar 

  • Smital T, Sauerborn R, Pivcevic B, Krca S, Kurelec B (2000) Interspecies differences in P-glycoprotein mediated activity of multixenobiotic resistance mechanism in several marine and freshwater invertebrates. Comp Biochem Physiol C Toxicol Pharmacol 126:175–186

    CAS  Google Scholar 

  • Smith AJ, van Helvoort A, van Meer G, Szabo K, Welker E, Szakacs G, Varadi A, Sarkadi B, Borst P (2000) MDR3 P-glycoprotein, a phosphatidylcholine translocase, transports several cytotoxic drugs and directly interacts with drugs as judged by interference with nucleotide trapping. J Biol Chem 275:23530–23539

    Article  CAS  Google Scholar 

  • Stevenson CN, MacManus-Spencer LA, Luckenbach T, Luthy RG, Epel D (2006) New perspectives on perfluorochemical ecotoxicology: inhibition and induction of an efflux transporter in the marine mussel, Mytilus californianus. Environ Sci Technol 40:5580–5585

    Article  CAS  Google Scholar 

  • Sturm A, Cunningham P, Dean M (2009) The ABC transporter gene family of Daphnia pulex. BMC Genomics 10

  • Takhteev VV (2000) Essays on Lake Baikal’s amphipods: systematics, comparative ecology, evolution. Irkutsk State University Press, Irkutsk

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • Timofeyev MA, Shatilina ZM, Bedulina DS, Menzel R, Steinberg CEW (2007) Natural organic matter (NOM) has the potential to modify the multixenobiotic resistance (MXR) activity in freshwater amphipods Eulimnogammarus cyaneus and E. verrucosus. Comp Biochem Phys B 146:496–503

    Article  CAS  Google Scholar 

  • Timofeyev MA, Protopopova M, Pavlichenko V, Steinberg CE (2009) Can acclimation of amphipods change their antioxidative response? Aquat Ecol 43:1041–1045

    Article  CAS  Google Scholar 

  • Timoshkin OA (2001) Lake Baikal: diversity of fauna, problems of its immiscibility and origin, ecology and “exotic” communities. In: Timoshkin OA (ed) Index of animal species inhabiting Lake Baikal and its catchment area. Nauka, Novosibirsk, pp 74–117

    Google Scholar 

  • Ueda K, Cardarelli C, Gottesman MM, Pastan I (1987) Expression of a full-length cDNA for the human “MDR1” gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci U S A 84:3004–3008

    Article  CAS  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3

  • Weiss RF, Carmack Carmack EC, Koropalov VM (1991) Deep-water renewal and biological production in Lake Baikal. Nature 349:665–669

    Article  CAS  Google Scholar 

  • Yoshioka T, Ueda S, Khodzher T, Bashenkhaeva N, Korovyakova I, Sorokovikova L, Gorbunova L (2002) Distribution of dissolved organic carbon in Lake Baikal and its watershed. Limnology 3:0159–0168

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was financially supported by scholarships from the Deutscher Akademischer Austauschdienst (DAAD) and the Russian Ministry of Education and Science (“Mikhail Lomonosov” Programme), by an international DAAD scholarship, by a Erasmus Mundus (MULTIC II) scholarship, and by the bilateral funding program “Helmholtz-Russia Joint Research Groups” (HRJRG) from the Helmholtz Association and the Russian Foundation for Basic Research (RFBR) (LabEglo project HRJRG-221). The authors particularly want to thank Dr. Nils Klüver for valuable advice, Benjamin Knoll and Mirko Pietsch for technical support in the lab, Ute Lohse for sequencing, Silke Aulhorn for phenanthrene analysis with HPLC, and Dr. Denis Axenov-Gribanov and students of Irkutsk State University for field sampling and exposure experiments. The authors also thank the crew of the scientific boat “Professor Kozhov” for help in organization of field expeditions; the Baikal Analytical Center for Collecting Use SB RAS; the heads of Irkutsk State University (A.V. Arguchintsev), Siberian Institute of Plant Physiology and Biochemistry (V.K. Voinikov and G.B. Borovskii), and Institute of Biology at Irkutsk State University (N.I. Granina) for financial and technical support of expedition work on Lake Baikal and financial support of Russian co-authors during the work under this manuscript. The experimental work on Lake Baikal and the salary of V.V. Pavlichenko and M.V. Protopopova during the study and work under the manuscript were partly supported by the Federal Target Program “Kadry” (Projects NK-267P and NK-366P) and by grants from the Russian Foundation for Basic Research (RFBR) no 14-04-31681 mol_a and no 14-04-31350 mol_a.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Till Luckenbach.

Additional information

Responsible editor: Cinta Porte

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pavlichenko, V.V., Protopopova, M.V., Timofeyev, M. et al. Identification of a putatively multixenobiotic resistance related Abcb1 transporter in amphipod species endemic to the highly pristine Lake Baikal. Environ Sci Pollut Res 22, 5453–5468 (2015). https://doi.org/10.1007/s11356-014-3758-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3758-y

Keywords

Navigation