Study of the influence of heavy metals on the microbiocenosis of Peter the Great bay of the Sea of Japan on the example of microalgae and bacteria under the conditions of a laboratory experiment

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Abstract

The influence of lead, cadmium, nickel, zinc and iron in concentrations corresponding to MPC and 2 MPC on the properties of Heterosigma akashiwo microalgae exometabolites in relation to bacteria isolated from different areas of the Peter the Great Bay of the Sea of Japan was evaluated. The results obtained showed metal resistance in 8 bacteria out of 18 tested. Different effects of exometabolites of Heterosigma akashiwo cultivated on heavy metals (HM) against bacteria resistant to these substances were found. Stimulation of the growth of opportunistic bacteria Vibrio sp., Escherichia sp., Escherichia coli, Staphylococcus lentus, Enterococcus sp., Staphylococcus pasteuri by exometabolites was revealed. In several cases, a decrease in the number of Pseudomonas sp. bacteria was recorded, with the addition of metabolites of microalgae grown with cadmium, lead and nickel at 10 and 20 µg/l, for Bacillus sp. at 20 µg/l lead, 10 µg/l and 20 µg/l cadmium, and also at 50 and 100 µg/l of iron. As a result, cadmium, lead and iron had the greatest effect on the effect of exometabolites on bacteria.

About the authors

Albina V. Ognistaya

Far Eastern Federal University; A.V. Zhirmunsky National Scientific Center of Marine Biology Far Eastern Branch, Russian Academy of Sciences (NSCMB FEB RAS)

Author for correspondence.
Email: alya_lokshina@mail.ru

Postgraduate Student

Russian Federation, Vladivostok

Tatyana I. Dunkai

Far Eastern Federal University;
A.V. Zhirmunsky National Scientific Center of Marine Biology Far Eastern Branch, Russian Academy of Sciences (NSCMB FEB RAS)

Email: tdunkai@yandex.ru

Postgraduate Student

Russian Federation, Vladivostok

Ivan G. Tananaev

Far Eastern Federal University

Email: geokhi@mail.ru

Corresponding Member RAS, Doctor of Chemical Sciences, Professor of the Department of Nuclear Technologies, Far Eastern Federal University

Russian Federation, Vladivostok

Zhanna V. Markina

A.V. Zhirmunsky National Scientific Center of Marine Biology Far Eastern Branch, Russian Academy of Sciences (NSCMB FEB RAS)

Email: zhannav@mail.ru

Candidate of Biological Sciences, Researcher, Laboratory of Cell Technologies

Russian Federation, Vladivostok

References

  1. Davis A., Shokouhian M., Shubei N. Loading estimates of lead, copper, cadmium, and zinc in urban runoff from specific sources // Chemosphere. 2001. № 44. R. 997-1009. EDN: AQWGAP
  2. Khristoforova, N.K. Sovremennoe ekologicheskoe sostoyanie zaliva Petra Velikogo Yaponskogo morya: monografiya / otvetstvennyy redaktor: N. K. Khristoforova. Dal'nevostochnyy federal'nyy universitet. - Vladivostok, 2012. - 440 s. EDN: QKUZXF
  3. Buzoleva, L.S. Mikrobiologicheskaya otsenka kachestva prirodnykh vod, letnyaya uchebno-polevaya praktika: ucheb. posob. / L.S. Buzoleva. - Vladivostok, 2011. - 88 s.
  4. Voronin, E.S. Veterinarnaya biologiya i immunologiya / E.S. Voronin, V.N. Kislenko, N.M. Kolychev // Elektronnyy didakticheskiy kompleks. - M., 2006. - URL: https://nsau.edu.ru/images/vetfac/images/ebooks/microbiology/stu/bacter/ecologia/toksbact.htm.
  5. Kachestvo morskikh vod po gidrokhimicheskim pokazatelyam. Ezhegodnik 2021. M.: Nauka, 2022. - 230 s.
  6. Kachestvo morskikh vod po gidrokhimicheskim pokazatelyam. Ezhegodnik 2019 [Pod red. Korshenko A.N.]. - M.: Nauka, 2020. - 232 s.
  7. Ramanan R., Kim B.H., Cho D.H. Algae-bacteria interactions: Evolution, ecology and emerging applications // Biotechnology Advances. 2016.Vol. 34. Is 1. P. 14-29. EDN: WSAHEN
  8. Fokina, A.I. Tyazhelye metally kak faktor izmeneniya metabolizma u mikroorganizmov (obzor) / A.I. Fokina, T.Ya. Ashchikhmina, L.I. Domracheva, E.A. Gornostaeva // Teoreticheskaya i prikladnaya ekologiya. - 2015. - №2. - S. 5-18. EDN: UFEZRN
  9. Kapkov, V.I. Ispol'zovanie morskikh odnokletochnykh vodorosley v biologicheskom monitoringe / V.I. Kapkov, E.V. Shoshina, O.A. Belenikina // Vestnik Murmanskogo gosudarstvennogo tekhnicheskogo universiteta. - 2017. - № 20(2). - S. 308-315. EDN: ZCHVLD
  10. Growth response of six strains of Heterosigmaakashiwo to varying temperature, salinity and irradiance conditions / R. Martínez, E. Orive, A.S. Laza-Martínez Seoane //j. Plankton Res. 2010. № 32. R. 529-538.
  11. Broad salinity tolerance as a refuge from predation in the harmful raphidophyte alga Heterosigmaakashiwo (Raphidophyceae) / S.L. Strom, E.L. Harvey, K.A. Fredrickson, S. Menden-Deuer //j. Phycol. 2013. №49. P. 20-31.
  12. Dursun F., Taş S., Koray T. Spring bloom of the raphidophycean Heterosigmaakashiwo in the golden horn estuary at the northeast of sea of marmara // Ege J. Fish. Aquat. Sci. 2016. Vol. 33. P. 201-207.
  13. Guillard R.R.L., Ryther J.H. Studies of marine planktonic diatoms. 1. Cyclotella nana Hustedt and Detonula con fervacea (Cleve) Gran // Canadian Journal of Microbiology. 1962.Vol.8. (2). P. 229-239.
  14. Comparison of several methods effective lipid extraction from microalgae /j.Y. Lee, C. Yoo, S.Y. Jun, C.Y. Ahn, H.M. Oh // Bioresour. Technol. 2010. №101. P. 75-77.
  15. The effect of microalgae extraction on bacterial species isolated from seminal fluid of sexually - active males in Baghdad / A. Hashimi, N. Shahrazad, R.F. Mansur //j. Genet. Environ. Resour. Conserv. 2016. №4 (2). P. 171-177.
  16. Christensen G.D., Simpson W.A., Younger J.J. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices // J Clin. Microbiology. 1985. №22 (6). P. 996 -1006.
  17. O'Toole G.A., Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis // Molecular Microbiology. 1998. Vol.28. №3. R. 449-461.
  18. Bruins M.R., Kapil S., Oehme F.W. Microbial resistance to metals in the environment // Ecotoxicol Environ Saf. 2000 Vol. 45 (3). P. 198-207.
  19. Bezverbnaya, I.P. Otklik mikroorganizmov pribrezhnykh akvatoriy Primor'ya na prisutstvie v srede tyazhelykh metallov: Avtoref. dis. … kand. biol. nauk / I.P. Bezverbnaya. - Vladivostok, 2002. - 18 s. EDN: QDTMKT
  20. Kumar M., Upreti R.K. Impact of lead stress and adaptation in Escherichia coli // Ecotoxicology and environmental safety. 2000. Vol. 47. Is.3. P. 246-252.
  21. Fashola M.O., Ngole-Jeme V.M., Babalola O.O. Heavy metal pollution from gold mines: Environmental effects and bacterial strategies for resistance // International journal of environmental research and public health. 2016. Vol. 13. №11. 1047 p. EDN: XZJPJX
  22. Bissen M., Frimmel F. Arsenic-a review. Part I: occurrence, toxicity, speciation, mobility // Acta hydrochimica et hydrobiologica. 2003. Vol. 31. №1. P. 9-18.
  23. Dovletyarova, E.A. Izmenenie biokhimicheskoy aktivnosti batsill pod vliyaniem svintsovogo zagryazneniya dernovo-podzolistoy pochvy / E.A. Dovletyarova // Dokl. TSKhA (Moskovskaya s.kh. akad. im. Timiryazeva). - 2004. - № 276. - S. 342-346.
  24. Sysoev, A.A. Vliyanie ionov svintsa i ROV na rost, razvitie i adenilatnyy energeticheskiy zaryad mikrovodorosley v kul'turakh / A.A. Sysoev, I.V. Sysoeva // Voprosy sovremennoy al'gologii. - 2017. - № 1(13). - 24 s. EDN: ZCDLUN
  25. Impact of heavy metals from flue gas integration with microalgae production / K. Napan, L. Teng, J.C. Quinn, B.D. Wood // Algal Res. 2015. №8. R. 83-88. EDN: UTTQFF
  26. Gopalakrishnan V., Ramamurthy D. Dyeing industry effluent system as lipid production medium of Neochloris sp. for biodiesel feedstock preparation // Biomed. Res.Int. 2014.R. 529-560.
  27. Effect of metals, metalloids and metallic nanoparticles on microalgae growth and industrial product biosynthesis: A Review / K. Miazek, W. Iwanek, C. Remacle, A. Richel, D. Goffin // Int J Mol Sci. 2015. Vol.16 (10). R.23929-69. EDN: TBMAYI
  28. Secondary metabolites production combined with lead bioremediation by Halamphora sp. marine diatom microalgae and their physiological response / D.B.I. Moussa, S. Boukhriss, K. Athmouni, H. Ayadi // Int J Aquac Fish Sci.2022. № 8 (2). R. 025-036.
  29. Tripathi V.N., Strivastova S. Ni2+-uptake in Pseudomonas putida strain S4: A possible role of Mg2+-uptake pump //j. Biosci. 2006. Vol. 31. № 1. P. 61-67.
  30. Paperi R., Micheletti E., Phillppis R. Optimizatiuon of copper sorbing-desorbing cycles with confined cultures of the exopolysaccaride-praducing cyanobacterium Cyanospiracapsulatan //j. Appl. Microbiol. 2006. Vol. 101. № 6. P. 1351-1356.
  31. Thomas M., Benov L. The contribution of superoxide radical to cadmium toxicity in E. coli // Biol. Trace Elem. Res. 2018. №181. R. 361-368. EDN: RTFHLK
  32. Cadmium pollution impact on the bacterial community structure of arable soil and the isolation of the cadmium resistant bacteria / Y. Xiaoxia, Z.J. Tong, L. Xiaoqing, S.L. Xin // Frontiers in Microbiology. 2021. Vol. 12. P. 1664-302X.
  33. Ecological responses of bacterial assembly and functions to steep Cd gradient in a typical Cd-contaminated farmland ecosystem / Y. Deng, S.D. Fu, E.K. Sarkodie, S.F. Zhang // Ecotoxicol Environ Saf. 2022. №229. 113067 r.
  34. Effects of Cd contamination on paddy soil microbial biomass and enzyme activities and rice physiological indices / L. Zeng, M. Liao, C. Huang, Y. Luo // Biodivers Sci. 2005. №13(6). R. 555-65.
  35. Peng Y., Xiaojie L., Jinhua L. Effects of cadmium stress on microbial community diversity in soil potted with sasa argentea striatus // IOP Conference Series: Earth and Environmental Science. 2019. 300 r.
  36. Effect of biochars and microorganisms on cadmium accumulation in rice grains grown in Cd-contaminated soil / P. Suksabye, A. Pimthong, P. Dhurakit, P. Mekvichitsaeng, P. Thiravetyan // Environ. Sci. Pollut. Res. 2016. №23. R. 962-973. EDN: AYSLRZ
  37. Somov, G.P. Adaptatsiya patogennykh bakteriy k abioticheskim faktoram okruzhayushchey sredy / G. P. Somov, L. S. Buzoleva. - Ros. akad. med. nauk. Sib. otd-nie, NII epidemiologii i mikrobiologii. - Vladivostok: Primpoligrafkomb., 2004. - 167 s. EDN: QKNBHR
  38. Effect of nickel on the fermentative growth of Escherichia coli k-12 and comparison of nickel and cobalt toxicity on the aerobic and anaerobic growth / L.F. Wu, C. Navarro, K. Pina, M. Quénard, M.A. Mandrand // Environmental health perspectives. 1994. Vol. 102. P. 297-300.
  39. Hausinger R.P., Zamble D.B. Microbial physiology of nikel and cobalt // Molecular microbiology of heavy metals / Eds. Nies Springer-Verlag. 2007.P. 287-320.
  40. Comparative genomics of regulation of heavy metal resistance in Eubacteria / E.A. Permina, A.E. Kazakov, O.V. Kalinina, M.S. Gelfand // BMC Microbiol. 2006. Vol.6. P. 49-60. EDN: LJVYDB
  41. Maier R.J., Benoit S.L. Role of nickel in microbial pathogenesis // Inorganics. 2019. Vol. 7(7). 80p. EDN: ZHYKSU
  42. Alboghobeish H., Tahmourespour A., Doudi M. The study of nickel resistant bacteria (NiRB) isolated from wastewaters polluted with different industrial sources // J Environ Health Sci Eng. 2014. Vol.12(1). 44 p. EDN: XYSPCY
  43. Akhmetov, L.I. Toksichnost' nikelya dlya tionovykh bakteriy / L.I. Akhmetov, A.G. Bykov, M.B. Vaynshteyn, T.Z. Esikova, A.E.Filonov, L.N. Krylova, S. Mortazavi // Izvestiya Tul'skogo gosudarstvennogo universiteta. Estestvennye nauki. - 2010. - Vol. (1). - P. 167-174. EDN: MUYVQL
  44. Hernandz B., Dorian A. Zinc and lead biosorption by Delftiatsuruhatensis: a bacterial strain resistant to metals isolated from mine tailings // J water Resource Protec. 2012. №4. P. 1-11.
  45. Rajbanshi A. Study on heavy metal resistant bacteria is Guhewori sewage treatment plant // J our nature. 2008. №6. P. 52-57.
  46. Arundhati P., Paul A.K. Nickel uptake and intracellular localization in Cupriaviduspauculuskps 201 // Adv bioscibiotechnol. 2010. №1. R. 276-280.
  47. Mohammady N.G., Fathy A.A. Humic acid mitigates viability reduction, lipids and fatty acids of Dunaliella salina and Nannochloropsissalina grown under nickel stress // Int. J. Bot. 2007. №3. R. 64-70. EDN: OZTKNX
  48. Responses of cyanobacterium Anabaena doliolum during nickel stress / M.K. Shukla, R.D. Tripathi, N. Sharma, S. Dwivedi, S. Mishra, R. Singh, O.P. Shukla, U.N. Rai //j. Environ. Biol. 2009. №30. R. 871-876.
  49. In vitro test of inhibition effect of extracts from three seaweed species distributed at Black Sea on different pathogens potentially dangerous for aquaponics / I. Sirakov, K. Velichkova, N.Rusenova, T. Dinev // Biotechnol Lett. 2019. Vol. 24 (1). P. 176-183.
  50. Oznobikhina, A.O. Model'noe biotestirovanie vliyaniya soley tyazhelykh metallov na zhiznesposobnost' kluben'kovykh bakteriy Rhizobiummeliloti / A.O. Oznobikhina, A.Yu. Pershakov, D.I. Eremin // Samarskiy nauchnyy vestnik. - 2019. - T. 8, - № 3 (28). - S. 69-72. EDN: WMABOE
  51. Korol'kova, D.S. Opredelenie minimal'nykh podavlyayushchikh kontsentratsiy soley tsinka na rost probioticheskikh shtammov bakteriy roda Bacillus / D.S. Korol'kova, M.L. Rusyaeva, I.V. Korobova // Mezhdunarodnyy studencheskiy nauchnyy vestnik. - 2018. - № 4. - 3 s. EDN: XPLFXN
  52. Pringault O., Viret H., Duran R.Interactions between Zn and bacteria in marine tropical coastal sediments // Environmental science and pollution research international. 2011. №19. R.879-92.
  53. Suryawati B. Zinc homeostasis mechanism and its role in bacterial virulence capacity // The 8th annual basic science international conference. AIP Conf. Proc. 2021. R. 070021-1-070021-7.
  54. El-Naggar A.H. Growth and some metabolic activities of Chlorella and Scenedesmus in relation to heavy metal pollution in Gharbia Governorate // Botany Department, Faculty of Science. 1993. 278 r.
  55. De-Filippis L.E., Hampp R., Ziegler H. The effects of sub-lethal concentrations of zinc, cadmium and mercury on Euglena growth and pigments // Planzen Physiol. 1981a. №101. R. 37-47.
  56. De-Filippis L.E., Hampp R., Ziegler H. The effects of sub-lethal concentrations of zinc, cadmium and mercury on Euglena II. Respiration, photosynthesis and photochemical activities // Arch Microbiol.1981b. R.128-404.
  57. Rai L.C., Singh A.K., Mallick N. Studies on photosynthesis, the associated electron transport system and some physiological variables of Chlorella vulgaris under heavy metal stress // J Plant Physiol.1991. №137. R. 419-424.
  58. Izuchenie mikroorganizmov, okislyayushchikh zhelezo, dlya vozmozhnogo ispol'zovaniya v biotekhnologii ochistki vody / K.T. Ngun, D.A. Raguzina, E.V. Pleshakova, M.V. Reshetnikov // Izvestiya Saratovskogo universiteta. Novaya seriya. Seriya: Khimiya. Biologiya. Ekologiya. 2018. T. 18, № 2. S. 204-210. EDN: UTKZRU
  59. Effects of iron limitation on growth and carbon metabolism in oceanic and coastal heterotrophic bacteria / M. Fourquez, A. Devez, A. Schaumann, A. Gueneugues, T. Jouenne // Limnology and Oceanography Bulletin. 2014. №59 (2). R. 349-360.
  60. Effect of iron concentration on the growth rate of Pseudomonas syringae and the expression of virulence factors in hrp-inducing minimal medium / B.J. Kim, J.H. Park, T.H. Park, P.A. Bronstein, D.J. Schneider, S.W. Cartinhour, M.L. Shuler // Appl Environ Microbiol. 2009. №75(9). R. 2720-6.
  61. Specific effect of trace metals on marine heterotrophic microbial activity and diversity: key role of iron and zinc and hydrocarbon-degrading bacteria / F. Baltar, A. Gutiérrez-Rodríguez, M. Meyer, I. Skudelny, S. Sander, B. Thomson, S. Nodder, R. Middag, S.E. Morales // Front Microbiol. 2018. №19. 3190 r.
  62. Microstructures and functional groups of Nannochloropsis sp. cells with arsenic adsorption and lipid accumulation /j. Cheng, Z. Yang, K. Li, J. Zhou, K. Cen // Bioresour. Technol. 2015. №194. R. 305-311. EDN: UTTQOB
  63. Effects of iron limitation on growth and carbon metabolism in oceanic and coastal heterotrophic bacteria / A. Devez, M. Fourquez, S. Blain, I. Obernosterer, A. Shaumann, Guéneuguès A., Jouenne T // Limnology and oceanography. 2014. №52. 349 r.
  64. The effect of iron on growth, lipid accumulation, and gene expression profile of the freshwater microalga Chlorella sorokiniana // M. Wan, X. Jin, J. Xia, J.N. Rosenberg, G. Yu, Z. Nie // Appl MicrobiolBiotechnol. 2014. № 98. R. 9473-9481. EDN: UTNRPP
  65. The effect of iron concentration on the growth rate of Chlamydomonas reinhardtii /j.C. Seo, J.F. Tang, M.J. Wagstaff // The Expedition. 2013. Vol. 3. R. 9-16.
  66. Yeesang C., Cheirsilp B. Effect of nitrogen, salt, and iron content in the growth medium and light intensity on lipid production by microalgae isolated from freshwater sources in Thailand // Biores Technol. 2011. №102. R. 3034-3040. EDN: OLPMVV
  67. Enhancement of lipid accumulation in Scenedesmus obliquus by optimizing CO2 and Fe3+ levels for biodiesel production / H.H.A. El-Baky, G.S. E.B. Bouaid, M. Martinez, J. Aracil // Biores Technol. 2012. №119. R. 429-432.
  68. Of iron valence on the growth, photosynthesis, and fatty acid composition of Phaeodactylumtricornutum / H. Wang, Q. Su, Y. Zhuang, C. Wu, S. Tong, B. Guan, Y. Zhao, H. Qiao //j. Mar. Sci. Eng. 2023. №11. 316 r.
  69. Influence of Fe+2 on the biomass, pigments, and essential fatty acids of Arthrospira platensis / M.M. El-Sheekh, J.M. Salman, R.A. Grmasha // Biomass Conv. Bioref. 2022.
  70. Rizwan M., Mujtaba G., Lee K. Effects of iron sources on the growth and lipid carbohydrate production of marine microalga Dunaliella tertiolecta // BiotechnolBioproc. 2017. № 22. R. 68-75.

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