Microalgae from eroded soils in the northern Fergana valley, Uzbekistan

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

For the first time, the cultivated diversity of microalgae in eroded soils in the northern part of the Fergana Valley in Uzbekistan has been studied based on both morphological and molecular genetic analysis. Ten strains of green microalgae (Chlorophyta) and one Charophyta strain were revealed. Only seven strains could be identified at the species level: Chlorella vulgaris, Chromochloris zofingiensis, Deuterostichococcus epilithicus, Pseudomuriella schumacherensis, and Pseudostichococcus monallantoides. Another four strains were identified only at the genus level and require further study: Bracteacoccus sp., Chlorosarcinopsis sp., Klebsormidium sp., and Tetratostichococcus sp. The low species diversity in the microalgae is likely due to both the low fertility of the eroded soils on the slopes, and the limitations of the culture-based approach that only reveals a fraction of the overall microbial diversity. Microalgal colonization of eroded soils in the arid foothill zone can be facilitated by various adaptations, such as small cell size and the production of extracellular polysaccharides, mycosporine-like aminoacids, and secondary carotenoids. The present work may contribute to the further development of highly functional microalgae-based consortia, which can lead to improvements and sustainable development of low-productivity, arid, and degraded terrestrial ecosystems.

Full Text

Restricted Access

About the authors

Yu. А. Tukhtaboeva

Namangan State University

Email: temraleeva.anna@gmail.com
Uzbekistan, Namangan

Е. S. Krivina

Pushchino Scientific Center for Biological Research, Russian Academy of Sciences

Email: temraleeva.anna@gmail.com

All-Russian Collection of Microorganisms (VKM), Skryabin Institute of Biochemistry and Physiology of Microorganisms

Russian Federation, Pushchino

V. V. Red’kina

Pushchino Scientific Center for Biological Research, Russian Academy of Sciences

Email: temraleeva.anna@gmail.com

All-Russian Collection of Microorganisms (VKM), Skryabin Institute of Biochemistry and Physiology of Microorganisms

Russian Federation, Pushchino

А. D. Temraleeva

Pushchino Scientific Center for Biological Research, Russian Academy of Sciences

Author for correspondence.
Email: temraleeva.anna@gmail.com

All-Russian Collection of Microorganisms (VKM), Skryabin Institute of Biochemistry and Physiology of Microorganisms

Russian Federation, Pushchino

References

  1. Андреева В. М. Почвенные и аэрофильные зеленые водоросли (Chlorophyta: Tetrasporales, Chlorococcales, Chlorosarcinales). СПб.: Наука, 1998. 351 с.
  2. Бут И. П. Почвенные водоросли некоторые районов Сурхандарийской области // Узбекский биологические журнал. 1959. № 2. С. 26–38.
  3. Дубовик И. Е. Влияние овражной эрозии на развитие водорослей в лесостепных почвах Предуралья // Почвоведение. 2004. № 4. С. 474–479.
  4. Dubovik I. E. The effect of gully erosion on the diversity of algae in forest-steppe soils of the cis-Ural region // Euras. Soil Sci. 2004. V. 37. P. 409‒414.
  5. Дубовик И. Е. Водоросли эродированных почв и альгологическая оценка почвозащитных мероприятий. Уфа: Изд-во Башкирского ун-та, 1995. 154 с.
  6. Киселев Е. И. Материалы к изучению микрофлоры рисовых полей окрестностей г. Самарканда // Журнал Русского ботанического общества. 1931. Т. 6. № 4. C. 20–22.
  7. Музафаров А. М. Флора водорослей водоемов Средней Азии. Ташкент: Изд-во “Наука” Узбекской ССР, 1965. 569 с.
  8. Мусаев К. Ю. Водоросли орошаемых земель и их значение для плодородия почв. Ташкент: Изд-во Академии Наук Узбекской ССР, 1960. 211 c.
  9. Мухамедиев А. М. Материалы к гидробиологии рисовых полей Ферганской долины // Ученые записки Ферган. пед. института. Сер. Биол. 1960. № 6. C. 3–75.
  10. Темралеева А. Д., Минчева Е. В., Букин Ю. С., Андреева А. М. Современные методы выделения, культивирования и идентификации зеленых водорослей (Chlorophyta). Кострома: Костромской печатный дом, 2014. 215 с.
  11. Троицкая Е. К. Водоросли основных почв юго-Западных Кызылкумов. Автореф. дис. … канд. биол. наук. Ташкент, 1961. 19 с.
  12. Тухтабоева Ю. А., Редькина В. В., Темралеева А. Д. Stichococcus-подобные микроводоросли (Trebouxiophyceae, Chlorophyta) в эродированных почвах Ферганской долины // Узбекский биологический журнал. 2023. № 4 (в печати).
  13. Умарова Ш. У. Водоросли хлопковых полей и влияние некоторых агротехнических факторов на развитие и распространение. Автореф. дис. … канд. биол. наук. Ташкент, 1964. 25 с.
  14. ФАО ООН. Европейская комиссия по сельскому хозяйству. 2015 // Продовольственная и сельскохозяйственная организация ООН. URL: https://www.fao.org/3/mo297r/mo297r.pdf (дата обращения: 24.11.2023).
  15. Büdel B., Darienko T., Deutschewitz K., Dojani S., Friedl T., Mohr K. I., Salisch M., Reisser W., Weber B. Southern African biological soil crusts are ubiquitous and highly diverse in drylands, being restricted by rainfall frequency // Microb. Ecol. 2009. V. 57. P. 229–247. https://doi.org/10.1007/s00248-008-9449-9
  16. Caisová L., Marin B., Melkonian M. A consensus secondary structure of ITS2 in the Chlorophyta identified by phylogenetic reconstruction // Protist. 2013. V. 164. P. 482–496. https://doi.org/10.1016/j.protis.2013.04.005
  17. Cardon Z. G., Gray D. W., Lewis L. A. The green algal underground: evolutionary secrets of desert cells // BioScience. 2008. V. 58. P. 114–122. https://doi.org/10.1641/B580206
  18. Castillo-Monroy A., Maestre F., Delgado-Baquerizo M., Gallardo A. Biological soil crusts modulate nitrogen availability in semi-arid ecosystems: insights from a Mediterranean grassland // Plant Soil. 2010. V. 333. P. 21–34. https://doi.org/10.1007/s11104-009-0276-7
  19. Chekanov K. Diversity and distribution of carotenogenic algae in Europe: a review // Mar. Drugs. 2023. V. 21. Art. 108. https://doi.org/10.3390/md21020108
  20. Coleman A. W. Is there a molecular key to the level of “biological species” in eukaryotes? A DNA guide // Mol. Phylogenet. Evol. 2009. V. 50. P. 197–203. https://doi.org/10.1016/j.ympev.2008.10.008
  21. Costa O. Y.A., Raaijmakers J. M., Kuramae E. E. Microbial extracellular polymeric substances: ecological function and impact on soil aggregation // Front. Microbiol. 2018. V. 9. Art. 1636. https://doi.org/10.3389/fmicb.2018.01636
  22. Ettl H., Gärtner G. Syllabus der Boden-, Luft- und Flechtenalgen. Stuttgart: Gustav Fischer, 1995. 721 p.
  23. Evans R. D., Johansen J. R. Microbiotic crusts and ecosystem processes // Crit. Rev. Plant Sci. 1999. V. 18. P. 183–225. https://doi.org/10.1080/07352689991309199
  24. Fischer T., Subbotina M. Climatic and soil texture threshold values for cryptogamic cover development: a meta analysis // Biologia (Bratisl.). 2014. V. 69. P. 1520–1530. https://doi.org/10.2478/s11756-014-0464-7
  25. Fucíková K., Lewis L. A. Intersection of Chlorella, Muriella and Bracteacoccus: resurrecting the genus Chromochloris Kol et Chodat (Chlorophyceae, Chlorophyta) // Fottea. 2012. V. 12. P. 83–93. https://doi.org/10.5507/fot.2012.007
  26. Fucíková K., Rada J. C., Lewis L. A. The tangled taxonomic history of Dictyococcus, Bracteacoccus and Pseudomuriella Chlorophyceae, Chlorophyta) and their distinction based on a phylogenetic perspective // Phycologia. 2011. V. 50. № 4. P. 422‒429. https://doi.org/10.2216/10-69.1
  27. Glaser K., Baumann K., Leinweber P., Mikhailyuk T. Karsten U. Algal richness in BSCs in forests under different management intensity with some implications for P cycling // Biogeosciences. 2018. V. 15. P. 4181–4192. https://doi.org/10.5194/bg-15-4181-2018
  28. Guiry M. D., Guiry G. M. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway, 2023. http://www.algaebase.org
  29. Hartmann A., Glaser K., Holzinger A., Ganzera M., Karsten U. Klebsormidin A and B, two new UV-sunscreen compounds in green microalgal Interfilum and Klebsormidium species (Streptophyta) from terrestrial habitats // Front. Microbiol. 2020 V. 11. Art. 499. https://doi.org/10.3389/fmicb.2020.00499
  30. Holzinger A., Kaplan F., Blaas K., Zechmann B., Komsic-Buchmann K., Becker B. Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense reaction // PLoS One. 2014. V. 9. Art. e110630. https://doi.org/10.1371/journal.pone.0110630
  31. Johnson J. L., Fawley M. W., Fawley K. P. The diversity of Scenedesmus and Desmodesmus (Chlorophyceae) in Itasa State Park, Minnesota, USA // Phycologia. 2007. V. 46. P. 214–229. https://doi.org/10.2216/05-69.1
  32. Karsten U., Friedl T., Schumann R., Hoyer K., Lembcke S. Mycosporine‐like amino acids and phylogenies in green algae: Prasiola and its relatives from the Trebouxiophyceae (Chlorophyta) // J. Phycol. 2005. V. 41. P. 557‒566. https://doi.org/10.1111/j.1529-8817.2005.00081.x
  33. Karsten U., Herburger K., Holzinger A. Living in biological soil crust communities of African deserts ‒ Physiological 20 traits of green algal Klebsormidium species (Streptophyta) to cope with desiccation, light and temperature gradients // J. Plant Physiol. 2016. V. 194. P. 2–12. https://doi.org/10.1016/j.jplph.2015.09.002
  34. Kitzing C., Pröschold T., Karsten U. UV-induced effects on growth, photosynthetic performance and sunscreen contents in different populations of the green alga Klebsormidium fluitans (Streptophyta) from alpine soil crusts // Microb. Ecol. 2014. V. 67. P. 327‒340. https://doi.org/10.1007/s00248-013-0317-x
  35. Krivina E. S., Bobrovnikova L. A., Temraleeva A. D., Markelova A. G., Gabrielyan D. A., Sinetova M. A. Description of Neochlorella semenenkoi gen. et sp. nov. (Chlorophyta, Trrebouxiophyceae), a novel Chlorella-like alga with high biotechnological potential // Diversity. 2023. V. 15. Art. 513. P. 1‒22. https://doi.org/10.3390/d15040513
  36. Langhans T. M., Storm C., Schwabe A. Community assembly of biological soil crusts of different successional stages in a temperate sand ecosystem, as assessed by direct determination and enrichment techniques // Microb. Ecol. 2009. V. 58. P. 394–407. https://doi.org/10.1007/s00248-009-9532-x
  37. Lu Q., Xiao Y., Lu Y. Employment of algae-based biological soil crust to control desertification for the sustainable development: a mini-review // Algal Res. 2022. V. 65. Art. 102747. https://doi.org/10.1016/j.algal.2022.102747
  38. Lukešová A. Soil algae in brown coal and lignite post-mining areas in Central Europe (Czech Republic and Germany) // Restor. Ecol. 2001. V. 9. P. 341–350. https://doi.org/10.1046/j.1526-100X.2001.94002.x
  39. Mamasoliev S. T. Soil algae of urban ecosystems (on the example of Andijan). Avtoreferat dis. Namangan, 2019. 25 p.
  40. McManus H.A., Lewis L. A. Molecular phylogenetic relationships in the freshwater family Hydrodictyaceae (Sphaeropleales, Chlorophyceae), with an emphasis on Pediatrum duplex // J. Phycol. 2011. V. 47. P. 152–163. https://doi.org/10.1111/j.1529-8817.2010.00940.x
  41. Metting B. The systematics and ecology of soil algae // Bot. Rev. 1981. V. 47. P. 195–312. https://doi.org/10.1007/BF02868854
  42. Mikhailyuk T., Glaser K., Holzinger A., Karsten U., Gabrielson P. Biodiversity of Klebsormidium (Streptophyta) from alpine biological soil crusts (Alps, Tyrol, Austria, and Italy) // J. Phycol. 2015. V. 51. P. 750–767. https://doi.org/10.1111/jpy.12316
  43. Mikhailyuk T., Glaser K., Tsarenko P., Demchenko E., Karsten U. Composition of biological soil crusts from sand dunes of the Baltic Sea coast in the context of an integrative approach to the taxonomy of microalgae and cyanobacteria // Eur. J. Phycol. 2019. V. 54. P. 263–290. https://doi.org/10.1080/09670262.2018.1557257
  44. Moewus L. Systematische Bestimmung einzelliger grüner Algen auf Grund von Kulturversuchen (Sphaerosorus composita, Oocystis marina und Pseudostichococcus monallantoides) // Botaniska Notiser. 1951. P. 287–318.
  45. Neustupa J., Eliás M., Sejnohová L. A taxonomic study of two Stichococcus species (Trebouxiophyceae, Chlorophyta) with a starch-enveloped pyrenoid // Nova Hedwigia. 2007. V. 84. P. 51–63. https://doi.org/10.1127/0029-5035/2007/0084-005
  46. Perera I., Subashchandrabose S. R., Venkateswarlu K., Naidu R., Megharaj M. Consortia of cyanobacteria/microalgae and bacteria in desert soils: an underexplored microbiota // Appl. Microbiol. Biotechnol. 2018. V. 102. P. 7351–7363. https://doi.org/10.1007/s00253-018-9192-1
  47. Pluis J. L.A. Algal crust formation in the inland dune area, Laarder Wasmeer, the Netherlands // Vegetatio. 1994. V. 113. P. 41–51. https://doi.org/10.1007/BF00045462
  48. Pröschold T., Darienko T. The green puzzle Stichococcus (Trebouxiophyceae, Chlorophyta): New generic and species concept among this widely distributed genus // Phytotaxa. 2020. V. 441. P. 113–142. https://doi.org/10.11646/phytotaxa.441.2.2
  49. Rabiei A., Zomorodian S. M.A., O’Kelly B. C. Reducing the erodibility of sandy soils engineered by cyanobacteria inoculation: a laboratory investigation // Sustainability. 2023. V. 15. Art. 3811. https://doi.org/10.3390/su15043811
  50. Rindi F., Mikhailyuk T. I., Sluiman H. J., Friedl T., López-Bautista J. M. Phylogenetic relationships in Interfilum and Klebsormidium (Klebsormidiophyceae, Streptophyta) // Mol. Phylogenet. Evol. 2011. V. 58. P. 218–231. https://doi.org/10.1016/j.ympev.2010.11.030
  51. Rippin M., Borchhardt N., Williams L., Colesie C., Jung P., Büdel B., Karsten U., Becker B. Genus richness of microalgae and Cyanobacteria in biological soil crusts from Svalbard and Livingston Island: morphological versus molecular approaches // Polar Biol. 2018. V. 41. P. 909–923. https://doi.org/10.1007/s00300-018-2252-2
  52. Rybalka N., Blanke M., Tzvetkova A., Noll A., Roos C., Boy J., Boy D., Nimptsch D., Godoy R., Friedl T. Unrecognized diversity and distribution of soil algae from Maritime Antarctica (Fildes Peninsula, King George Island) // Front. Microbiol. 2023. V. 14. Art. 118747. https://doi.org/10.3389/fmicb.2023.1118747
  53. Samolov E., Mikhailyuk Y., Lukešová A., Glaser K. Büdel B., Karsten U. Usual alga from unusual habitats: biodiversity of Klebsormidium (Klebsormidiophyceae, Streptophyta) from the phylogenetic superclade G isolated from biological soil crusts // Mol. Phyl. Evol. 2019. V. 133. P. 236–255. https://doi.org/10.1016/j.ympev.2018.12.018
  54. Seitz S., Nebel M., Goebes P., Käppeler K., Schmidt K., Shi X., Song Z., Webber C. L., Weber B., Scholten T. Bryophyte-dominated biological soil crusts mitigate soil erosion in an early successional Chinese subtropical forest // Biogeosci. 2017. V. 14. P. 5775–5788. https://doi.org/10.5194/bg-14-5775-2017
  55. Sommer V., Karsten U., Glaser K. Halophilic algal communities in biological soil crusts isolated from potash tailings pile areas // Front. Ecol. Evol. 2020. V. 8. Art. 46. https://doi.org/10.3389/fevo.2020.00046
  56. Van A. T., Glaser K. Pseudostichococcus stands out from its siblings due to high salinity and desiccation tolerance // Phycology. 2022. V. 2. P. 108–119. https://doi.org/10.3390/phycology2010007
  57. Xiao R., Zheng Y. Overview of microalgal extracellular polymeric substances (EPS) and their applications // Biotechnol. Adv. 2016. V. 34. P. 1225–1244. https://doi.org/10.1016/j.biotechadv.2016.08.004

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. Photographs of the sampling sites for soil and algological samples and a map of the study areas of eroded soils in the northern part of the Fergana Valley indicating the sampling points.

Download (471KB)
3. Fig. 2. Photographs of microalgae strains isolated from eroded soils of the Fergana Valley: a – Klebsormidium sp. ACSSI 436; b – Chlorosarcinopsis sp. ACSSI 445, the inset shows zoospores, the arrow points to the mucus; c – Tetratostichococcus sp. ACSSI 446; d – Chlorella vulgaris ACSSI 441; d – Pseudostichococcus monallantoides ACSSI 438, arrows point to oil droplets; f ‒ P. monallantoides ACSSI 439; g – Chromochloris zofingiensis ACSSI 437; h – Pseudomuriella schumacherensis ACSSI 444; i – Deuterostichococcus epilithicus ACSSI 440; k – Bracteacoccus sp. ACSSI 443. Scale mark ‒ 10 µm.

Download (501KB)
4. Fig. 3. Rooted phylogenetic tree of charophyte microalgae of the genus Klebsormidium constructed by the Bayesian method based on the sequences of the plastid gene rbcL (1255 nt). SH-aLRT/BP/PP values ​​are given as statistical support for tree nodes. SH-aLRT and BP values ​​less than 70% and PP less than 0.7 are not given. Nucleotide substitution model: TIM2 + F + I + G4. Designations: * ‒ authentic strains; (T) – type species.

Download (580KB)
5. Fig. 4. Rooted phylogenetic tree of the studied green microalgae of the genus Chlorosarcinopsis, constructed by the Bayesian method based on the sequences of the internal transcribed spacer ITS2 (284 nt). SH-aLRT/BP/PP values ​​are indicated as statistical support for tree nodes. SH-aLRT and BP values ​​less than 70% and PP less than 0.7 are not indicated. Nucleotide substitution model: TIM2e + G4. Designations: * ‒ authentic strains.

Download (541KB)
6. Fig. 5. Rooted phylogenetic tree of green microalgae Stichococcus-clade constructed by the Bayesian method based on the sequences of the internal transcribed spacer ITS2 (375 nt). SH-aLRT/BP/PP values ​​are given as statistical support for tree nodes. SH-aLRT and BP values ​​less than 70% and PP less than 0.7 are not given. Nucleotide substitution model: HKY + F+ G4. Designations: * ‒ authentic strains; (T) – type species.

Download (439KB)
7. Fig. 6. Rooted phylogenetic tree of green microalgae of the Chlorella clade constructed by the Bayesian method based on the sequences of the internal transcribed spacer ITS2 (287 nt). SH-aLRT/BP/PP values ​​are given as statistical support for tree nodes. SH-aLRT and BP values ​​less than 70% and PP less than 0.7 are not given. Nucleotide substitution model: TIM2 + F + I + G4. Designations: * ‒ authentic strains; (T) – type species.

Download (793KB)
8. Fig. 7. Rooted phylogenetic trees of green microalgae of the genera Chromochloris (a) and Pseudomuriella (b) constructed by the Bayesian method based on the sequences of the internal transcribed spacer ITS2 (321 and 280 nt, respectively). SH-aLRT/BP/PP values ​​are given as statistical support for tree nodes. SH-aLRT and BP values ​​less than 70% and PP less than 0.7 are not given. The nucleotide substitution model is TIM2 + G4 and TNe + G4, respectively. Designations: * ‒ authentic strains; (T) – type species.

Download (432KB)
9. Fig. 8. Rooted phylogenetic tree of green microalgae of the genus Bracteacoccus constructed by the Bayesian method based on the sequences of the internal transcribed spacer ITS2 (347 nt). SH-aLRT/BP/PP values ​​are given as statistical support for tree nodes. SH-aLRT and BP values ​​less than 70% and PP less than 0.7 are not given. Nucleotide substitution model: GTR + F + G4. Designations: * ‒ authentic strains; (T) – type species.

Download (552KB)
10. Additional materials

Download (295KB)

Copyright (c) 2024 Russian Academy of Sciences