Skip to main content
Log in

Environmental Factors Associated with the Eukaryotic Microbial Diversity of Ulleungdo Volcanic Island in South Korea

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Ulleungdo is a volcanic island with an oceanic climate seasonally affected by warm and cold currents. The freshwater ecosystems of Ulleungdo Island act as an ecological indicator that reveals changes caused by various environmental factors. This study applied Illumina MiSeq to analyze microalgal groups within the eukaryotic microbial community and determine regional differences in microalgal groups inhabiting Ulleungdo Island. Also, we compared the Illumina MiSeq analysis with the culture-based analysis results. The 18S rRNA regions were amplified using an 18S V4 primer set to analyze eukaryotic microbial and microalgal communities. As a result, Basidiomycota (fungi) was the predominant eukaryotic microbial group. The proportion of Chlorophyta (green algae) in the microalgal group was higher than that of Bacillariophyta (diatoms). The microalgal species detected included two diatoms (Achnanthidium minutissimum and Nitzschia palea) and three green algae (Dictyosphaerium spp., Tetradesmus obliquus, and Desmodesmus spp.). Additionally, the composition and species diversity of eukaryotic microbial communities changed according to the environmental factors of each stream or groundwater source. Illumina MiSeq analysis is a powerful tool for overcoming the limitations of culture-based analyses. Therefore, our research provided an enhanced ecological understanding of environmental factors associated with microalgal groups within the eukaryotic microbial community of Ulleungdo Island.

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

REFERENCES

  1. Admas, A., Sahile, S., Agidie, A., Menale, H., Gedefaw, T., and Teshome, M., Controlling water hyacinth infestation in Lake Tana using fungal pathogen from laboratory level up to pilot scale, bioRxiv., 2020. https://doi.org/10.1101/2020.01.14.901140

  2. Alain, K. and Querellou, J., Cultivating the uncultured: limits, advances and future challenges, Extremophiles, 2009, vol. 13, pp. 583–594.

    Article  Google Scholar 

  3. Al-Harbi, S., Seasonal dynamics and community composition of epilithic microalgae in relation with environmental factors at northwest coast of Jeddah: the Red Sea, Oceanogr. Mar. Biol., 2017, vol. 5, pp. 1–8.

    CAS  Google Scholar 

  4. Andrade, D.S., Amaral, H.F., Gavilanes, F.Z., Morioka, L.R.I., Nassar, J.M., de Melo, J.M., Silva, H.R., and Telles, T.S., Microalgae: cultivation, biotechnological, environmental, and agricultural applications, in Advances in the Domain of Environmental Biotechnology, Mad-dela, N.R., García Cruzatty, L.C., and Chakraborty, S., Eds., Springer, 2021, pp. 635–701.

    Google Scholar 

  5. Chen, W., Zhang, C.K., Cheng, Y., Zhang, S., and Zhao, H., A comparison of methods for clustering 16S rRNA sequences into OTUs, PLoS One, 2013, vol. 8, no. 8, e70837.

    Article  CAS  Google Scholar 

  6. Claassen, S., du Toit, E., Kaba, M., Moodley, C., Zar, H.J., and Nicol, M.P., Comparison of the efficiency of five different commercial DNA extraction kits for extraction of DNA from faecal samples, J. Microbiol. Methods., 2013, vol. 94, no. 2, pp. 103–110.

    Article  CAS  Google Scholar 

  7. Delgado, C. and Pardo, I., Comparison of benthic diatoms from Mediterranean and Atlantic Spanish streams: community changes in relation to environmental factors, Aquat. Bot., 2015, vol. 120, pp. 304–314.

    Article  Google Scholar 

  8. Devi, S.G., Fathima, A.A., Radha, S., Arunraj, R., Curtis, W.R., and Ramya, M., A rapid and economical method for efficient DNA extraction from diverse soils suitable for metagenomic applications, PLoS One, 2015, vol. 10, no. 7, p. e0132441.

    Article  Google Scholar 

  9. Elshobary, M.E., Essa, D.I., Attiah, A.M., Salem, Z.E., and Qi, X., Algal community and pollution indicators for the assessment of water quality of Ismailia canal, Egypt, Stoch. Environ. Res. Risk. Assess., 2020, vol. 34, pp. 1089–1103.

    Article  Google Scholar 

  10. Fábregas, J., Domínguez, A., Regueiro, M., Maseda, A., and Otero, A., Optimization of culture medium for the continuous cultivation of the microalga Haematococcus pluvialis, Appl. Microbiol. Biotechnol., 2000, vol. 3. art. 5, pp. 530–535.

  11. Fawley, M.W. and Fawley, K.P., Identification of eukaryotic microalgal strains, J. Appl. Phycol., 2020, vol. 32, art. 5, pp. 2699–2709.

  12. Fouhy, F., Deane, J., Rea, M.C., O’Sullivan, Ó., Ross, R.P., O’Callaghan, G., Plant, B.J., and Stanton, C., The effects of freezing on faecal microbiota as determined using MiSeq sequencing and culture-based investigations, PLoS One., 2015, vol. 10, art. 3, p. e0119355.

  13. Galès, A., Triplet, S., Geoffroy, T., Roques, C., Carré, C., Le Floc’h, E., Lanfranchi, M., Simier, M., d’Orbcastel, E.R., Przybyla, C., and Fouilland, E., Control of the pH for marine microalgae polycultures: a key point for CO2 fixation improvement in intensive cultures, J. CO2 Util., 2020, vol. 38, pp. 187–193.

  14. Garus-oas, C.H. and Julies, E., Seasonal relative abundance and diversity of microalgae in freshwater eutrophic systems of Namibia, J. Cell. Biotechnol., 2020, vol. 6, art. 1, pp. 57–70.

  15. Gessner, M., Gulis, V., Kuehn, K., Chauvet, E., and Suberkropp, K., Fungal decomposers of plant litter in aquatic ecosystem, Environ. Microb. Relatsh., 2007, vol. 4, pp. 301–324.

    Google Scholar 

  16. Gressel, J., van der Vlugt, C.J., and Bergmans, H.E., Environmental risks of large scale cultivation of microalgae: mitigation of spills, Algal Res., 2013, vol. 2, art. 3, pp. 286–298.

  17. Grover, J.P., Resource competition and community structure in aquatic micro-organisms: experimental studies of algae and bacteria along a gradient of organic carbon to inorganic phosphorus supply, J. Plankton Res., 2000, vol. 22, art. 8, pp. 1591–1610.

  18. Harris, N., Harvey, K.V., Gordon, S.C., Alderman, P., Esposito, D., Reif, J.S., and Schaefer, A.M., Algal bloom–related illness: improving health outcomes in primary care, J. Nurse Pract., 2020, vol. 16, art. 9, pp. 679–682.

  19. Hayashi, H., Sakamoto, M., and Benno, Y., Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods, Microbiol. Immunol., 2002, vol. 46, art. 8, pp. 535–548.

  20. Hillebrand, H. and Sommer, U., Diversity of benthic microalgae in response to colonization time and eutrophication, Aquat. Bot., 2000, vol. 67, art. 3, pp. 221–236.

  21. Huang, W., Li, B., Zhang, C., Zhang, Z., Lei, Z., Lu, B., and Zhou, B., Effect of algae growth on aerobic granulation and nutrients removal from synthetic wastewater by using sequencing batch reactors, Bioresour. Technol., 2015, vol. 179, pp. 187–192.

    Article  CAS  Google Scholar 

  22. Jung, S.Y., Park, S.H., Nam, C.H., Lee, H.J., Lee, Y.M., and Chang, K.S., The distribution of vascular plants in Ulleungdo and nearby island regions (Gwaneumdo, Jukdo), J. Asia Pac. Biodivers., 2013, vol. 6, art. 1, pp. 123–156.

  23. Karthik, R., Robin, R., Anandavelu, I., Purvaja, R., Singh, G., Mugilarasan, M., Jayalakshmi, T., Samuel, V.D., and Ramesh, R., Diatom bloom in the Amba River, west coast of India: a nutrient-enriched tropical river-fed estuary, Reg. Stud. Mar. Sci., 2020, vol. 35, p. 101244.

    Google Scholar 

  24. Kim, C.H., Park, J.W., Lee, M.H., and Park, C.H., Detailed bathymetry and submarine terraces in the coastal area of the Dokdo volcano in the Ulleung Basin, the East Sea (Sea of Japan), J. Coast. Res., 2013, vol. 65, pp. 523–528.

    Article  Google Scholar 

  25. Kim, K., Mun, H., Shin, H., Park, S., Yu, C., Lee, J., Yoon, Y., Chung, H., Yun, H., and Lee, K., Nitrogen stimulates Microcystis-dominated blooms more than phosphorus in river conditions that favor non-nitrogen-fixing genera, Environ. Sci. Technol., 2020, vol. 54, art. 12, pp. 7185–7193.

  26. Kim, Y.-S., Yun, H.-S., Lee, J.-H., Kim, H.-S., and Yoon, H.-S., Environmental factors associated with the eukaryotic microbial community and microalgal groups in the mountain marshes of South Korea, Pol. J. Microbiol., 2021, vol. 70, art. 2, p. 215.

  27. Kozich, J.J., Westcott, S.L., Baxter, N.T., Highlander, S.K., and Schloss, P.D., Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform, Appl. Environ. Microbiol., 2013, vol. 79, art. 17, pp. 5112–5120.

  28. Kruse, G.O., Shafii, B., Hoyle, G.M., Holderman, C., and Anders, P.J., Changes in primary producer and consumer communities in response to upstream nutrient addition in the Kootenai river, Idaho, Northwest Sci., 2020, vol. 93, art. 3–4, pp. 226–243.

  29. Kwon, D., A geomorphology on the Ulleungdo, J. Korean Geomorphological Assoc., 2012, vol. 19, pp. 39–57.

    Google Scholar 

  30. Lee, Y.G., Kim, B.J., Park, G.U., and Ahn, B.Y., Characteristics of precipitation and temperature at Ulleung-do and Dok-do, Korea for recent four years (2005~2008), J. Environ. Sci. Int., 2010, vol. 19, art. 9, pp. 1109–1118.

  31. Li, H., Barber, M., Lu, J., and Goel, R., Microbial community successions and their dynamic functions during harmful cyanobacterial blooms in a freshwater lake, Water. Res., 2020, vol. 185, p. 116292.

    Article  CAS  Google Scholar 

  32. Lines, T., Orr, P., and Beardall, J., Elevated CO2 has differential effects on five species of microalgae from a subtropical freshwater lake: possible implications for phytoplankton species composition, J. Phycol, 2021, vol. 57, no. 1, pp. 324−334. https://doi.org/10.1111/jpy.13104

  33. Liu, Y., Li, N., Lou, Y., Zhao, X., and Wang, G., Effect of water accommodated fractions of fuel oil on fixed carbon and nitrogen by microalgae: implication by stable isotope analysis, Ecotoxicol. Environ. Saf., 2020, vol. 195, p. 110488.

    Article  CAS  Google Scholar 

  34. Li, W., Fu, L., Niu, B., Wu, S., and Wooley, J., Ultrafast clustering algorithms for metagenomic sequence analysis, Brief. Bioinform., 2012, vol. 13, art. 6, pp. 656–668.

  35. Lombard, N., Prestat, E., van Elsas, J.D., and Simonet, P., Soil-specific limitations for access and analysis of soil microbial communities by metagenomics, FEMS Microbiol. Ecol., 2011, vol. 78, art. 1, pp. 31–49.

  36. Ludley, K.E. and Robinson, C.H., ‘Decomposer’ basidiomycota in Arctic and Antarctic ecosystems, Soil Biol. Biochem., 2008, vol. 40, art. 1, pp. 11–29.

  37. Maberly, S.C., Pitt, J.-A., Davies, P.S., and Carvalho, L., Nitrogen and phosphorus limitation and the management of small productive lakes, Inland Waters, 2020, vol. 10, art. 2, pp. 159–172.

  38. Meeranayak, U.F.J., Nadaf, R.D., Toragall, M.M., and Nadaf, U., The role of algae in sustainable environment: a review, J. Algal. Biomass. Util., 2020, vol. 11, pp. 28–34.

    Google Scholar 

  39. Mercado, J.M., Cortés, D., Gómez-Jakobsen, F., García-Gómez, C, Ouaissa, S, Yebra, L, Ferrera, I, Valcárcel-Pérez, N, López, M, and García-Muñoz, R., Role of small-sized phytoplankton in triggering an ecosystem disruptive algal bloom in a Mediterranean hypersaline coastal lagoon, Mar. Pollut. Bull., 2021, vol. 164, p. 111989.

    Article  CAS  Google Scholar 

  40. Meyer, M. and Kircher, M., Illumina sequencing library preparation for highly multiplexed target capture and sequencing, Cold Spring Harb Protoc., 2010, vol. 6, pdb. prot5448.

  41. Nam, H.K., Song, Y.J., Kwon, S.I., Eo, J., Yoon, S.S., Kwon, B.K., and Kim, M.H., Characteristics of ground-dwelling invertebrate communities at Nari Basin and Tonggumi area in Ulleungdo Island, J. Environ Biol., 2018, vol. 36, art. 1, pp. 21–32.

  42. Namsaraev, Z., Melnikova, A., Komova, A., Ivanov, V., Rudenko, A., and Ivanov, E., Algal bloom occurrence and effects in Russia, Water, 2020. vol. 12, art. 1, p. 285.

  43. Nirmala, N., Phylogenetic analysis for identification of lipid enriched microalgae and optimization of extraction conditions for biodiesel production using response surface methodology tool, Biocatal. Agric. Biotechnol., 2020, vol. 25, p. 101603.

    Article  Google Scholar 

  44. Nugroho, R., The oil-producing microalga Botryococcus braunii: a method for isolation from the natural environment and perspectives on the role of ecological studies in algal biofuel production, J. Ecosys. Ecograph., 2020, vol. 10, art. 3, p. 274.

  45. Poretsky, R., Rodriguez-R, L.M., Luo, C., Tsementzi, D., and Konstantinidis, K.T., Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics, PLoS One., 2014, vol. 9, art. 4, p. e93827.

  46. Rodríguez-Miranda, E., Acién, F.G., Guzmán, J.L., Berenguel, M., and Visioli, A., A new model to analyze the temperature effect on the microalgae performance at large scale raceway reactors, Biotechnol. Bioeng., 2020, vol. 118, pp. 877–889.

    Article  Google Scholar 

  47. Royer, T.V., Stoichiometry of nitrogen, phosphorus, and silica loads in the Mississippi-Atchafalaya River basin reveals spatial and temporal patterns in risk for cyanobacterial blooms, Limnol. Oceanogr., 2020, vol. 65, art. 2, pp. 325–335.

  48. Ryan, K., Hegseth, E., Martin, A., Davy, S., O’Toole, R., Ralph, P., McMinn, A., and Thorn, C., Comparison of the microalgal community within fast ice at two sites along the Ross Sea coast, Antarctica, Antarct. Sci., 2006, vol. 18, art. 4, pp. 583–594.

  49. Sánchez-Zurano, A., Ciardi, M., Lafarga, T., Fernández-Sevilla, J.M., Bermejo, R., and Molina-Grima, E., Role of microalgae in the recovery of nutrients from pig manure, Processes, 2021, vol. 9, art. 2, p. 203.

  50. Schleyer, G. and Vardi, A., Algal blooms, Curr. Biol., 2020, vol. 30, art. 19, pp. R1116–R1118.

  51. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., and Robinson, C.J., Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities, Appl. Environ. Microbiol., 2009, vol. 75, art. 23, pp. 7537–7541.

  52. Shokralla, S., Spall, J.L., Gibson, J.F., and Hajibabaei, M., Next-generation sequencing technologies for environmental DNA research, Mol. Ecol., 2012, vol. 21, art. 8, pp. 1794–1805.

  53. Slocombe, S.P., Zúñiga-Burgos, T., Chu, L., Wood, N.J., Camargo-Valero, M.A., and Baker, A., Fixing the broken phosphorus cycle: wastewater remediation by microalgal polyphosphates, Front. Plant. Sci., 2020, vol. 11, p. 982.

    Article  Google Scholar 

  54. Sohn, Y., Geology of Tok Island, Korea: eruptive and depositional processes of a shoaling to emergent island volcano, B. Volcanol., 1995, vol. 56, art. 8, pp. 660–674.

  55. Song, C., Han, X., Qiu, Y., Liu, Z., Li, S., and Kitamura, Y., Microalgae carbon fixation integrated with organic matters recycling from soybean wastewater: effect of pH on the performance of hybrid system, Chemosphere, 2020, vol. 248, p. 126094.

    Article  CAS  Google Scholar 

  56. Stanier, R., Kunisawa, R., Mandel, M., and Cohen-Bazire, G., Purification and properties of unicellular blue-green algae (order Chroococcales), Bacteriol. Rev., 1971, vol. 35, art. 2, p. 171.

    Article  CAS  Google Scholar 

  57. Stoeck, T., Bass, D., Nebel, M., Christen, R., Jones, M.D., Breiner, H.W., and Richards, T.A., Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water, Mol. Ecol., 2010, vol. 19, pp. 21–31.

    Article  CAS  Google Scholar 

  58. Sturm, M., Schroeder, C., and Bauer, P., SeqPurge: highly-sensitive adapter trimming for paired-end NGS data, BMC Bioinformat., 2016, vol. 17, art. 1, p. 208.

  59. Sutherland, D.L., Burke, J., Leal, E., and Ralph, P.J., Effects of nutrient load on microalgal productivity and community composition grown in anaerobically digested food-waste centrate, Algal. Res., 2020, vol. 51, p. 102037.

    Article  Google Scholar 

  60. Sutherland, D.L., Turnbull, M.H., and Craggs, R.J., Environmental drivers that influence microalgal species in fullscale wastewater treatment high rate algal ponds, Water Res., 2017, vol. 124, pp. 504–512.

    Article  CAS  Google Scholar 

  61. Tarvainen, O., Saravesi, K., Pennanen, T., Markkola, A.M., Suokas, M., and Fritze, H., Fungal communities in decomposing wood along an energy wood harvest gradient, Forest Ecol. Manag., 2020, vol. 465, p. 118070.

    Article  Google Scholar 

  62. Teittinen, A., Kallajoki, L., Meier, S., Stigzelius, T., and Soininen, J., The roles of elevation and local environmental factors as drivers of diatom diversity in subarctic streams, Freshwater Biol., 2016, vol. 61, art. 9, pp. 1509–1521.

  63. Tester, P.A., Litaker, R.W., and Berdalet, E., Climate change and harmful benthic microalgae, Harmful Algae., 2020, vol. 91, p. 101655.

    Article  Google Scholar 

  64. Umer, K., Ebenezer, V., and Subramoniam, T., A short-term study on the effect of environmental factor variation on a zooplankton community, Indian. J. Mar. Sci., 2020, vol. 49, art. 7, pp. 1158−1164.

  65. Vo, A.T. and Jedlicka, J.A., Protocols for metagenomic DNA extraction and Illumina amplicon library preparation for faecal and swab samples, Mol. Ecol. Resour., 2014, vol. 14, art. 6, pp. 1183–1197.

  66. Wyatt, K.H. and Stevenson, R.J., Effects of acidification and alkalinization on a periphytic algal community in an Alaskan wetland, Wetlands, 2010, vol. 30, art. 6, pp. 1193–1202.

  67. Yun, H.-S., Kim, Y.-S., and Yoon, H.-S., Illumina MiSeq analysis and comparison of freshwater microalgal communities on Ulleungdo and Dokdo islands, Pol. J. Microbiol., 2019, vol. 68, art. 4, p. 527.

  68. Yun, H.-S., Kim, Y.-S., Yoon, H.-S., Characterization of Chlorella sorokiniana and Chlorella vulgaris fatty acid components under a wide range of light intensity and growth temperature for their use as biological resources, Heliyon, 2020, vol. 6, art. 7, p. e04447.

  69. Zhang, H., Hou, F., Xie, W., Wang, K., Zhou, X., Zhang, D., and Zhu, X., Interaction and assembly processes of abundant and rare microbial communities during a diatom bloom process, Environ. Microbiol., 2020a, vol. 22, art. 5, pp. 1707–1719.

  70. Zhang, H., Zong, R., He, H., Liu, K., Yan, M., Miao, Y., Ma, B., and Huang, X., Biogeographic distribution patterns of algal community in different urban lakes in China: insights into the dynamics and co-existence, J. Environ. Sci., 2021, vol. 100, pp. 216–227.

    Article  CAS  Google Scholar 

  71. Zhang, J., Shu, X., Zhang, Y., Tan, X., and Zhang, Q., The responses of epilithic algal community structure and function to light and nutrients and their linkages in subtropical rivers, Hydrobiologia, 2020b, vol. 847, art. 3, pp. 841–855.

  72. Zhang, Z., Schwartz, S., Wagner, L., and Miller, W., A greedy algorithm for aligning DNA sequences, J. Comput. Biol., 2000c, vol. 7, art. 1–2, pp. 203–214.

  73. Zhou, J., Lao, Y.M., Song, J.T., Jin, H., Zhu, J.M., and Cai, Z.H., Temporal heterogeneity of microbial communities and metabolic activities during a natural algal bloom, Water. Res., 2020, vol. 183, p. 116020.

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the Basic Science Research Program of the National Research Foundation of Korea (NRF) funded by the Ministry of Education (Grant no. 2016R1A6A1A05011910, 2018R1D1A3B07049385 and 2021R1I1A205551711), Korea.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to H. S. Kim, Y. S. Kim or H. S. Yoon.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

* These authors contributed equally to this work.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yun, H.S., Lee, J.H., Choo, Y.S. et al. Environmental Factors Associated with the Eukaryotic Microbial Diversity of Ulleungdo Volcanic Island in South Korea. Microbiology 91, 801–817 (2022). https://doi.org/10.1134/S0026261721100568

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261721100568

Keywords:

Navigation