Identification of filamentous green algae from an area of local biogenic pollution of Lake Baikal (Listvennichnyy bay) using SSU 18S rDNA molecular marker

Abstract

Background. A local eutrophication process is noted for the first time in Listvennichnyi bay in Lake Baikal. High level of biogenic elements in the water of the bay led to nuisance growth of filamentous algae. Rapid identification of these algae's taxa was necessary to assess ecosystem damage in the polluted area of the lake. Materials and methods. We determined a boundary of bottom fouling by locating transects ranging from 0 to 10 meters in different areas of the bay. Algae samples were examined using microscopic techniques as well as SSU 18S rDNA sequencing. Phylogenetic trees were estimated using Bayesian inference (BI) based on SSU alignment. Results. Our results showed intensive filamentous algae fouling in depth from 3 to 10 meters along the coastline of the eastern part of the bay. Morphological and molecular analysis demonstrated prevalence in samples of Ulothrix zonata (Web. et Mohr) Kütz. Using SSU 18S rDNA sequencing data we also showed presence of three species of Spirogyra Link. genus. Conclusion. Detection of Spirogyra species which are normally not typical for such areas of the lake along with Ulothrix zonata extended more deeply than usually observed reveals severe phytocenosis disturbance of the polluted part of Lake Baikal.

Keywords

eutrophication / filamentous algae / molecular analysis / molecular marker / SSU

References

[1] Ижболдина Л. А. (1985) Количественное распределение эндемичных видов макрофитов вдоль открытых побережий оз. Байкал, Под ред. Галазия Г. И. Круговорот вещества и энергии в водоемах: Структура и продуктивность растительных сообществ (фитопанктон, фитобентос, высшая водная растительность). Вып. 2. Иркутск; c. 31-32.

[2] Ижболдина Л. А. (1990) Мейо- и макрофитобентос озера Байкал (водоросли). Иркутск: Изд-во ИГУ.

[3] Ижболдина Л. А. (2007) Атлас и определитель водорослей бентоса и перифитона озера Байкал (мейо- и макрофиты) с краткими очерками по их экологии. Новосибирск: Наука-Центр.

[4] Кравцова Л. С., Ижболдина Л. А., Ханаев И. В. и др. (2012) Нарушение вертикальной зональности зеленых водорослей в прибрежной части залива Лиственничный озера Байкал. ДАН. Т. 447(2): C. 227-229.

[5] Покровская Т. Н., Миронова Н. Я., Шилькрот Г. С. (1983) Макрофитные озера и их евтрофирование. М.: Наука.

[6] Рундина Л. А. (1998) Зигнемовые водоросли России (Chlorophyta: Zygnematophyceae, Zygnematales). СПб: Наука.

[7] Algal culturing techniques (2005) In Andersen R. A., editor. San Diego: Academic Press.

[8] Andreakis N., Procaccini G., Kooistra W. H. C. F. (2004) Asparagopsis taxiformis and Asparagopsis armata (Bonnemaisoniales, Rhodophyta): genetic and morphological identification of Mediterranean populations. Eur. J. Phycol. V. 39: P. 273-283.

[9] Auer M. T., Tomlinson L. M., Higgins S. N., et al. (2010) Great Lakes Cladophora in the 21st century: same algae-different ecosystem. J. Great Lakes Res. V. 36: P. 248-255.

[10] Buchheim M. A., Keller A., Koetschan C. et al. (2011) Internal transcribed spacer 2 (nu ITS2 rRNA) sequence-structure phylogenetics: towards an automated reconstruction of the green algal tree of life. PLoS One. V. 6(2): e16931.

[11] Chen C., Barfuss M. H., Pröschold T., et al. (2012) Hidden genetic diversity in the green alga Spirogyra (Zygnematophyceae, Streptophyta). BMC Evol. Biol. V. 12: P. 1-13.

[12] Depew D. C., Houben A. J., Guildford S. J., Hecky R. E. (2011) Distribution of nuisance Cladophora in the lower Great Lakes: Patterns with land use, near shore water quality and dreissenid abundance. J. Great Lakes Res. V. 37: P. 656-671.

[13] Doyle J. J., Dickson E. (1987) Preservation of plant samples for DNA restriction endonuclease analysis. Taxon. V. 36: P. 715-722.

[14] Drummond C. S., Hall J., Karol K. G., Delwiche C. F. (2005) Phylogeny of Spirogyra and Sirogonium (Zygnematophyceae) based on rbcL sequence data. J. Phycol. V. 41: P. 1055-1064.

[15] Friedl T. (1996) Evolution of the polyphyletic genus Pleurastrum (Chlorophyta): inferences from nuclear-encoded ribosomal DNA sequences and motile cell ultrastructure. Phycologia. V. 35: P. 456-469.

[16] Gontcharov A. A., Marin B. A., Melkonian M. A. (2003) Molecular phylogeny of conjugating green algae (Zygnemophyceae, Streptophyta) inferred from SSU rDNA sequence comparisons. J. Mol. EV. V. 56: P. 89-104.

[17] Hayden H.vS., Waaland J. R. (2002) Phylogenetic systematics of the Ulvaceae (Ulvales, Ulvophyceae) using chloroplast and nuclear and DNA sequences. J. Phycol. V. 38: P. 1200-1212.

[18] Hebert P. D., Cywinska A., Ball S. L., et al. (2003) Biological identifications through DNA barcodes. Proc. Biol. Sci. V. 270: P. 313-321.

[19] Higgings S. N., Hecky R. E., Guildford S. J. (2005) Modeling the growth, biomass, and tissue phosphorus concentration of Cladophora glomerata in eastern Lake Erie: Model description and field testing. J. Great Lakes Res. V. 31: P. 439-455.

[20] Hiraoka M., Ichihara K., Zhu W., et al. (2011) Culture and hybridization experiments on an Ulva clade including the Qingdao strain blooming in the Yellow Sea. Plos One. V. 6(5): P. 1-6.

[21] Hoshaw R. W. (1980) Systematics of the Zygnemataceae (Chlorophyceae). II. Zygospore wall structure in Sirogonium and a taxonomic proposal. J. Phycol. V. 16: P. 242-250.

[22] Hoshaw R. W., Wang J-C., McCourt R. M., et al. (1985) Ploidal changes in clonal cultures of Spirogyra communis and implications for species definition. Am. J. Bot. V. 72(7): P. 1005-1011.

[23] Hull H. M., Hoshaw R. W., Wang J-C. (1985) Interpretation of zygospore wall structure and taxonomy of Spirogyra and Sirogonium (Zygnemataceae, Chlorophyta). Phycologia. V. 24(2): P 231-239.

[24] Huson D. H., Bryant D. (2006) Application of Phylogenetic Networks in Evolutionary Studies. Mol. Biol. EV. V. 23(2): P. 254-267.

[25] Ikegaya H., Nakase T., Iwata K., et al. (2012) Studies on conjugation of Spirogyra using monoclonal culture. J. Plant Res. V. 125: P. 457-464.

[26] Katana A., Kwiatowski J., Spalik K., Zakrys B. (2001) Phylogenetic position of Koliella (Chlorophyta) as inferred from nuclear and chloroplast small subunit rDNA. J. Phycol. V. 37: P. 443-451.

[27] Kim J. H., Kim Y. H., Cho G. Y., Boo S. M. (2006) Plastid rbcL gene phylogeny of the genus Spirogyra (Chlorophyta, Zygnemataceae) from Korea. Korean J. Genet. V. 28: P. 295-303.

[28] Leliaert F., De Clerck O., Verbruggen H., et al. (2007) Molecular phylogeny of the Siphonocladales (Chlorophyta: Cladophorophyceae). Mol. Phylogenet. EV. V. 44 (3): P. 1237-1256.

[29] Leliaert F., Boedeker C., Pena V., et al. (2009) Cladophora rhodolithicola sp. nov. (Cladophorales, Chlorophyta), a diminutive species from European maerl beds.Europ. Journal Phycol. V. 44(2): P. 155-169.

[30] Lowe R. L., Pillsbury R. W. (1995) Shifts in benthic algal community structure and function following the appearance of zebra mussels (Dreissena polymorpha) in Saginaw Bay, Lake Huron. J. Great Lakes Res. V. 21 (4): P. 558-566.

[31] Mohapatra P. K., Mohanty R. C. (1992) Determination of water quality of two water bodies using algal bioassaymethod. Phycos. V. 31 (1, 2): P. 77-84.

[32] Nozaki K., Darijav K., Akatsuka T., et al. (2003) Development of green algae in the benthic algal community in a littoral sand-beach zone of Lake Biwa. Limnol. V. 4: P. 161-165.

[33] Ostendorp W., Schmieder K., Jöhnk K. (2004) Assessment of human pressures and their hydromorphological impacts on lake shores in Europe. Ecohydrol. Hydrobiol. V. 4: P. 379-395.

[34] Pang S. J., Liu F., Shan T. F., et al. (2010) Tracking the algal origin of the Ulva bloom in the Yellow Sea by a combination of molecular, morphological and physiological analyses. Mar. Environ. Res. V. 69(4): P. 207-215.

[35] Posada D. (2008) jModelTest: phylogenetic model averaging. Mol. Biol. EV. V. 25: P. 1253-1256.

[36] Prasanna R., Ratha S. K., Rojas C., et al. (2011) Algal diversity in flowing waters at an acidic mine drainage “barrens” in central Pennsylvania, USA. Folia Microbiol. (Praha). V. 56(6): P. 491-496.

[37] Rai U. N., Dubey S., Shukla O. P., et al. (2008) Screening and identification of early warning algal species for metal contamination in fresh water bodies polluted from point and non-point sources. Environ. Monit. Assess. V. 144(1, 3): P. 469-481.

[38] Ronquist F., Teslenko M., van der Mark P., et al. (2011) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. V. 61(3): P. 539-542.

[39] Saunders G. W., Kucera H. (2010) An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogamie, Algologie. V. 31(4): P. 487-528.

[40] Simons J., Van Beem A. P., de Vries P. J. R. (1984) Induction of conjugation and spore formation in species of Spirogyra, Chlorophyceae, Zygnematales. Acta Bot. Neerl. V. 33: P. 323-334.

[41] Skubinna J. P., Coon T. G., Batterson T. R. (1995) Increased abundance and depth of submersed macrophytes in response to decreased turbidity in Saginaw Bay, Lake Huron. J. Great Lakes Res. V. 21: P. 476-488.

[42] Smith V. H., Tilman G. D., Nekola J. C. (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ. Pollut. V. 100(1): P. 179-196.

[43] Smith V. H., Joye S. B., Howarth R. W. (2006) Eutrophication of freshwater and marine ecosystems. Limnol. Oceanogr. V. 51: P. 351-355.

[44] Stabenau H., Säftel W. (1989) Induction of conjugation in Mougeotia. Canad. J. Bot. V. 67(7). P. 2217-2218.

[45] Tamura K., Peterson D., Peterson N., et al. (2011) MEGA5: Molecular evolutionary genetics analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony methods. Mol. Biol. EV. V. 28: P. 2731-2739.

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Romanova E.V., Kravtsova L.S., Izhboldina L.A., Khanaev I.V., Sherbakov D.Y.