Taxonomic Composition of Cultured Fe-and Mn-Oxidizing Bacteria and Microbial Abundance in Fe-Mn Nodules of Different Sizes

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Abstract

Taxonomic diversity and quantitative distribution of cultured forms of Fe-and Mn-oxidizing microorganisms in Fe-Mn nodules of different sizes and fine earth of Gleyic Luvisols formed in the territory not affected by direct anthropogenic impact, were analyzed. The results were obtained using a combination of microbiological, molecular and analytical methods and noninvasive techniques. Most of the microorganisms which were cultured from the nodules were Mn oxidizers. Bacteria of the genera Bacillus, Rhodococcus, Lysinibacillus, Pseudomonas, and Priestia were identified in the nodules. Quantitative distribution of Fe-and Mn-oxidizing microorganisms in the outer and inner zones of the nodules of different sizes demonstrated that Mn-oxidizing microorganisms were involved in all stages of nodules formation and development, while Fe-oxidizing microorganisms participated in the initial phase of their formation. Spherules and porous structures of bacterial nature were observed in the studied nodules. The host fine earth was characterized by differences in the relative abundance of the dominant microbial groups in the profile. Manganese-oxidizing bacteria were represented in the soil fine earth by the genera Prestia and Methylobacterium.

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About the authors

Ya. О. Timofeeva

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences

Email: martynenko98@inbox.ru
Russian Federation, Vladivostok

E. S. Martynenko

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences; Far Eastern Federal University

Author for correspondence.
Email: martynenko98@inbox.ru
Russian Federation, Vladivostok; Vladivostok

M. L. Sidorenko

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences

Email: martynenko98@inbox.ru
Russian Federation, Vladivostok

A. V. Kim

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences; Far Eastern Federal University

Email: martynenko98@inbox.ru
Russian Federation, Vladivostok; Vladivostok

V. M. Kazarin

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences

Email: martynenko98@inbox.ru
Russian Federation, Vladivostok

References

  1. Аристовская Т. В. Роль микроорганизмов в мобилизации и закреплении железа в почвах // Почвоведение. 1975. № 4. С. 290–295.
  2. Астафьева М. М., Жегалло Е. А., Ривкина Е. М., Самылина О. С., Розанов А. Ю., Зайцева Л. В., Авдонин В. В., Карпов Г. А., Сергеева Н. Е. Бактериальная палеонтология. М.: Российская академия наук, 2021. 124 с.
  3. Водяницкий Ю. Н. Гидроксиды железа в почвах // Почвоведение. 2010. № 11. С. 1341–1352.
  4. Vodyanitskii Y. N. Iron hydroxides in soils: a review of publications // Euras. Soil Sci. 2010. V. 43. P. 1244–1254. https://doi.org/10.1134/S1064229310110074
  5. Зайдельман Ф. Р., Никифорова А. С. Генезис и диагностическое значение новообразований почв лесной и лесостепной зон. М.: МГУ им. М. В. Ломоносова, 2001. 216 с.
  6. Захарова, Ю.Р., Парфенова В. В. Метод культивирования микроорганизмов, окисляющих железо и марганец в донных отложениях озера Байкал // Известия РАН. Сер. биол. 2007. № 3. С. 290–295.
  7. Звягинцев Д. Г. Методы почвенной микробиологии и биохимии. М.: МГУ, 1991. 304 с.
  8. Классификация и диагностика почв России. Смоленск: Ойкумена, 2004. 342 с.
  9. Костенков Н. М. Окислительно-восстановительные режимы в почвах периодического переувлажнения (Дальний Восток). М.: Наука, 1986.
  10. Логинова О. О., Данг Т. Т., Белоусова Е. В., Грабович М. Ю. Использование штаммов рода Acinetobacter для биоремедиации нефтезагрязненных почв на территории Воронежской области // Вестник ВГУ. Серия: Химия. Биология. Фармация. 2011. № 2. С. 127–133.
  11. Лысак В. В. Микробиология. Минск: БГУ, 2007. 426 с.
  12. Лысак Л. В., Кадулин М. С., Конова И. А., Лапыгина Е. В., Иванов А. В., Звягинцев Д. Г. Численность, жизнеспособность и таксономический состав наноформ бактерий в железо-марганцевых конкрециях // Почвоведение. 2013. № 6. С. 707–714.
  13. Lysak L. V., Kadulin M. S., Konova I. A., Lapygina E. V., Ivanov A. V., Zvyagintsev D. G. Population number, viability, and taxonomic composition of the bacterial nanoforms in iron-manganic concretions // Euras. Soil Sci. 2013. V. 46. P. 668–675. https://doi.org/10.1134/S1064229313060069
  14. М-02-0604-2007. Методика выполнения измерений массовой доли кремния, кальция, титана, ванадия, хрома, бария, марганца, железа, никеля, меди, цинка, мышьяка, стронция, свинца, циркония, молибдена, в порошковых пробах почв и донных отложений рентгеноспектральным методом с применением энергодисперсионных рентгенофлуоресцентных спектрометров типа EDX фирмы “Shimadzu”. СПб., 2007. 17 с.
  15. Мартынова М. В. Формы нахождения марганца, их содержание и трансформация в пресноводных отложениях // Экологическая химия. 2012. Т. 21. С. 38–52.
  16. Пиневич А. В. Микробиология железа и марганца. СПб.: СПбГУ, 2005. 374 с.
  17. Пуртова Л. Н., Тимофеева Я. О. Изучение некоторых свойств и активности каталазы агротемногумусовых подбелов при различных видах агротехнического воздействия // Почвоведение. 2022. № 10. С. 1277–1289.
  18. Purtova L. N., Timofeeva Ya. O. Study of some properties and catalase activity in albic stagnosols under different agrogenic impacts // Euras. Soil Sci. 2022. V. 55. P. 1436–1445. https://doi.org/10.1134/S1064229322100131
  19. Пуртова Л. Н., Тимофеева Я. О. Характеристика мелкозема и ортштейнов агрогенных почв южной части Приморского края: физико-химические, оптические свойства, каталазная и каталитическая активность // Почвоведение. 2021. № 12. С. 1481–1491.
  20. Purtova L. N., Timofeeva Y. O. Fine earth and nodules in agrogenic soils from the south of Primorskii region: physicochemical and optical properties, catalase and catalytic activity // Euras. Soil Sci. 2021. V. 54. P. 1855–1863. https://doi.org/10.1134/S1064229321120097
  21. Росликова В. И. Марганцево–железистые новообразования в почвах равнинных ландшафтов гумидной зоны. Владивосток: Дальнаука, 1996. 291 с.
  22. Тимофеева Я. О. Накопление и фракционирование микроэлементов в почвенных железо-марганцевых конкрециях различного размера // Геохимия. 2008. № 3. С. 293–301.
  23. Timofeeva Y. O. Accumulation and fractionation of trace elements in soil ferromanganese nodules of different size // Geochem. Int. 2008. V. 46. P. 260–267. https://doi.org/10.1134/S0016702908030038
  24. Тимофеева Я. О., Голов В. И. Аккумуляция микроэлементов в ортштейнах почв // Почвоведение. 2010. № 4. С. 434–444.
  25. Timofeeva Y. O., Golov V. I. Accumulation of microelements in iron nodules in concretions in soils: a review // Euras. Soil Sci. 2010. V. 43. P. 401–407. https://doi.org/10.1134/S1064229310040058
  26. Федорюк Е. Д., Няникова Г. Г. Выделение культур железо- и марганец-окисляющих микроорганизмов // Наука и образование в современной конкурентной среде. 2015. № 1. С. 3–8.
  27. Холопов Ю. А. Изучение реакции микроорганизмов почв лесных ценозов на внесение солей свинца и кадмия в условиях модельного опыта // Известия Самарского научного центра РАН. 2013. Т. 15. С. 260–267.
  28. Щапова Л. Н. Микрофлора почв юга Дальнего востока России. Владивосток: ДВО РАН, 1994. 186 с.
  29. Ainiwaer A., Liang Y., Ye X., Gao R. Characterization of a novel Fe2+ activated non-blue laccase from Methylobacterium extorquens // Int. J. Mol. Sci. 2022. V. 23. Art. 9804. https://doi.org/10.3390/ijms23179804
  30. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI–BLAST: a new generation of protein database search programs // Nucl. Acids Res. 1997. V. 25. Р. 3389–3402. https://doi.org/10.1093/nar/25.17.3389
  31. Andreini C., Bertini I., Cavallaro G., Holliday G. L., Thornton J. M. Metal ions in biological catalysis: from enzyme databases to general principles // J. Biol. Inorg. Chem. 2008. V. 13. P. 1205–1218. https://doi.org/10.1007/s00775-008-0404-5
  32. Cappelletti M., Presentato A., Piacenza E., Firrincieli A., Turner R. J., Zannoni D. Biotechnology of Rhodococcus for the production of valuable compounds // Appl. Microbiol. Biotechnol. 2020. V. 104. P. 8567–8594. https://doi.org/10.1007/s00253-020-10861-z
  33. Ciancio C. L., Piazza A., Masotti F., Garavaglia B. S., Ottado J., Gottig N. Manganese oxidation counteracts the deleterious effect of low temperatures on biofilm formation in Pseudomonas sp. MOB-449 // Front. Mol. Biosci. 2022. V. 9. Art. 1015582. https://doi.org/10.3389/fmolb.2022.1015582.
  34. Cornu S., Deschatrettes V., Salvador-Blanes S., Clozul B., Hardy M., Branchut S., Forestier L. L. Trace element accumulation in Mn-Fe-oxide nodules of a planasolic horizon // Geoderma. 2005. V. 125. P. 11–24. https://doi.org/10.1016/j.geoderma.2004.06.009
  35. Cotroneo S., Schiffbauer J. D., McCoy V.E., Wortmann U. G., Darroch S. A., Peng Y., Laflamme M. A new model of the formation of Pennsylvanian iron carbonate concretions hosting exceptional soft-bodied fossils in Mazon Creek, Illinois // Geobiology. 2016. V. 14. P. 543–555. https://doi.org/10.1111/gbi.12197
  36. Dabard M. P., Loi A. Environmental control on concretion-forming processes: examples from Paleozoic terrigenous sediments of the North Gondwana margin, Armorican Massif (Middle Ordovician and Middle Devonian) and SW Sardinia (Late Ordovician) // Sediment. Geol. 2012. V. 267–268. P. 93–103. https://doi.org/10.1016/j.sedgeo.2012.05.013
  37. Dourado M. N., Camargo Neves A. A., Santos D. S., Araújo W. L. Biotechnological and agronomic potential of endophytic pink-pigmented methylotrophic Methylobacterium spp. // BioMed Res. Int. 2015. Art. 909016. https://doi.org/10.1155/2015/909016.
  38. Emenike C. U., Agamuthu P., Fauziah S. H. Blending Bacillus sp., Lysinibacillus sp. and Rhodococcus sp. for optimal reduction of heavy metals in leachate contaminated soil // Environ. Earth Sci. 2016. V. 75. Art. 26. https://doi.org/10.1007/s12665-015-4805-9
  39. Ettler V., Chren M., MihaljevičM., Drahota P., Kříbek B., Veselovský F., Sracek O., Vaněk A., Penížek V., Komárek M., Mapani B., Kamona F. Characterization of Fe-Mn concentric nodules from Luvisol irrigated by mine water in a semi-arid agricultural area // Geoderma. 2017. V. 299. P. 32–42. https://doi.org/10.1016/j.geoderma.2017.03.022
  40. Fischel M. H.H., Clarke C. E., Sparks D. L. Synchrotron resolved microscale and bulk mineralogy in manganese-rich soils and associated pedogenic concretions // Geoderma. 2023. V. 430. Art. 116305. https://doi.org/10.1016/j.geoderma.2022.116305
  41. Frawley E. R., Fang F. C. The ins and outs of bacterial iron metabolism // Mol. Microbiol. 2014. V. 93. P. 609–616. https://doi.org/10.1111/mmi.12709
  42. Gasparatos D. Fe-Mn concretions and nodules to sequester heavy metals in soils // Environ. Chem. Sust. World. 2012. V. 2. P. 443–474. https://doi.org/10.1007/978-94-007-2439-6_11
  43. Gasparatos D., Massas I., Godelitsas A. Fe-Mn concretions and nodules formation in redoximorphic soils and their role on soil phosphorus dynamics: current knowledge and gaps // Catena. 2019. V. 182. Art. 104106. https://doi.org/10.1016/j.catena.2019.104106
  44. Ghosh P. K., Maiti T. K., Pramanik K., Ghosh S. K., Mitra S., De T. K. The role of arsenic resistant Bacillus aryabhattai MCC3374 in promotion of rice seedlings growth and alleviation of arsenic phytotoxicity // Chemosphere. 2018. V. 211. P. 407–419. https://doi.org/10.1016/j.chemosphere.2018.07.148
  45. Gupta R. S., Patel S., Saini N., Chen S. Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species // Int. J. Syst. Evol. Microbiol. 2020. V. 70. P. 5753–5798. https://doi.org/10.1099/ijsem.0.004475
  46. Hu C., Zhang Y., Zhang L., Luo W. Effects of microbial iron reduction and oxidation on the immobilization and mobilization of copper in synthesized Fe(III) minerals and Fe-rich soils // J. Microbiol. Biotechnol. 2013. V. 24. P. 534–544. https://doi.org/10.4014/jmb.1310.10001
  47. Hu M., Li F., Lei J., Fang Y., Tong H., Wu W., Liu C. Pyrosequencing revealed highly microbial phylogenetic diversity in ferromanganese nodules from farmland // Environ. Sci. Process. Impacts. 2015. V. 17. P. 213–224. https://doi.org/10.1039/c4em00407h
  48. Jofré I., Matus F., Mendoza D., Nájera F., Merino C. Manganese-oxidizing Antarctic bacteria (Mn-Oxb) release reactive oxygen species (ROS) as secondary Mn(II) oxidation mechanisms to avoid toxicity // Biology. 2021. V. 10. Art. 1004. https://doi.org/10.3390/biology10101004
  49. Kepkay P. E., Nealson K. H. Growth of a manganese oxidizing Pseudomonas sp. in continuous culture // Arch. Microbiol. 1987. V. 148. P. 63–67. https://doi.org/10.1007/BF00429649
  50. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms // Mol. Biol. Evol. 2016. V. 35. P. 1547–1549. https://doi.org/10.1093/nar/25.17.3389
  51. Lane D. J., Pace B., Olsen G. J., Stahl D. A., Sogin M. L., Pace N. R. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses // Proc. Natl. Acad. Sci. USA. 1985. V. 82. Р. 6955–6959. https://doi.org/10.1073/pnas.82.20.6955
  52. Li J., Guo Y. K., Zhao Q. X., He J. Z., Zhang Q., Cao H. Y., Liang C. Q. Microbial cell wall sorption and Fe-Mn binding in rhizosphere contribute to the obstruction of cadmium from soil to rice // Front. Microbiol. 2023. V. 14. Art. 1162119. https://doi.org/10.3389/fmicb.2023.1162119
  53. Li-Mei Z., Liu F., Tan W., Feng X., Zhu Y., He J. Microbial DNA extraction and analyses of soil iron–manganese nodules // Soil Biol. Biochem. 2008. V. 40. P. 1364–1369. https://doi.org/10.1016/j.soilbio.2007.01.004
  54. Liu C., Massey M. S., Latta D. E., Xia Y., Li F., Gao T., Hua J. Fe(II)-induced transformation of iron minerals in soil ferromanganese nodules // Chem. Geol. 2021. V. 559. Art. 119901. https://doi.org/10.1016/j.chemgeo.2020.119901
  55. Lysak L., Konova I., Lapygina E., Soina V., Chekin M. Filtered forms of prokaryotes and bacteriophages in soil concretions // IOP Conf. Ser. Earth Environ. Sci. 2019. V. 368. Art. 012030. https://doi.org/10.1088/1755-1315/368/1/012030
  56. Lyu J., Yu X., Jiang M., Cao W., Saren G., Chang F. The mechanism of microbial-ferromanganese nodule interaction and the contribution of biomineralization to the formation of oceanic ferromanganese nodules // Microorganisms. 2021. V. 9. Art. 1247. https://doi.org/10.3390/microorganisms9061247
  57. Powell M. M., Rao G., Britt R. D., Rittle J. Enzymatic hydroxylation of aliphatic c-h bonds by a Mn/Fe cofactor // bioRxiv: the preprint server for biology. 2023. Art. 532131. https://doi.org/10.1101/2023.03.10.532131
  58. Schulz M. S., Vivit D., Schulz Ch., Fitzpatrick J., White. A. Biologic origin of iron nodules in a marine terrace chronosequence, Santa Cruz, California // Soil Sci. Soc. Am. J. 2010. V. 74. P. 550–564. https://doi.org/10.2136/sssaj2009.0144
  59. Shahid M., Zeyad M. T., Syed A., Singh U. B., Mohamed A., Bahkali A. H., Elgorban A. M., Pichtel J. Stress-tolerant endophytic isolate Priestia aryabhattai BPR-9 modulates physio-biochemical mechanisms in wheat (Triticum aestivum L.) for enhanced salt tolerance // Int. J. Environ. Res. Public Health. 2022. V. 19. Art. 10883. https://doi.org/10.3390/ijerph191710883
  60. Singh R., Grigg J. C., Qin W., Kadla J. F., Murphy M. E., Eltis, L. D. Improved manganese-oxidizing activity of DypB, a peroxidase from a lignolytic bacterium // ACS Chem. Biol. 2013. V. 8. P. 700–706. https://doi.org/10.1021/cb300608x
  61. Sipos P., Kovacs I., Balazs R., Toth A., Barna G., Mako A. Micro-analytical study of the distribution of iron phases in ferromanganese nodules // Geoderma. 2022. V. 405. Art. 115455. https://doi.org/10.1016/j.geoderma.2021.115445
  62. Suhr M., Raff J., Pollmann K. Au-interaction of Slp1 polymers and monolayer from Lysinibacillus sphaericus JG-B53 — QCM-D, ICP-MS and AFM as tools for biomolecule-metal studies // J. Vis. Exp. 2016. V. 107. Art. e53572. https://doi.org/10.3791/53572
  63. Tan W. F., Liu F., Li Y. H., Hu H. Q., Huang Q. Y. Elemental composition and geochemical characteristics of iron-manganese nodules in main soils of China // Pedosphere. 2006. V. 16. P. 72–81. https://doi.org/10.1016/S1002-0160(06)60028-3
  64. Timofeeva Y. O., Karabtsov A., Ushkova, M., Burdukovskii M., Semal V. Variation of trace element accumulation by iron-manganese nodules from Dystric Cambisols with and without contamination // J. Soils Sediments. 2021. V. 21. P. 1064–1078. https://doi.org/10.1007/s11368-020-02814-w
  65. Timofeeva Y. O., Karabtsov A. A., Semal’ V.A., Burdukovskii M. L., Bondarchuk N. V. Iron-manganese nodules in udepts: the dependence of the accumulation of trace elements on nodule size // Soil Sci. Soc. Am. J. 2014. V. 78. P. 767–778. https://doi.org/10.2136/sssaj2013.10.0444
  66. Zhang L. M., Liu F., Tan W. F., Feng X. H., ZhuY., He J. Microbial DNA extraction and analyses of soil iron-manganese nodules // Soil Biol. Biochem. 2008. V. 40. P. 1364–1369. https://doi.org/10.1016/j.soilbio.2007.01.004

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2. Fig. 1. Numbers of Mn-oxidising (a) and Fe-oxidising (b) microorganisms in soil fine soil

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3. Fig. 2. Phylogenetic tree constructed on the basis of sequence analysis of 16S rRNA gene fragment fragments of bacteria isolated from soil fine soil and orthosteins. The dendrogram was constructed based on the nearest neighbour (NJ) pooling method algorithm. Sequences obtained in this work are shown in bold. Bootstrap support values above 50% are presented

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4. Fig. 3. Maps of element distribution in the ortsteins

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5. Fig. 4. Structures in orthosteins: a - spherulas in the inner zone of orthosteins; b - group of spherulas on the surface of orthostein; c - elemental composition of spherulas; d - glycocalyx; e - ‘nanoflowers’ (nanoflowers)

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