Research Article
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Bacterial Biodiversity of the Kapova Karst Cave as a Source of Hydrolases Producers

Year 2023, , 186 - 195, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1349885

Abstract

Objective: Recent studies have revealed the biodiversity of both cultivated and uncultivated microbiomes in extreme environments. It has been shown that terrestrial subsurface ecosystems contain vast metabolic potential. Heterotrophic bacteria living in karst caves with an organic substrate deficit represent a special reserve for the isolation of metabolite producers. Here, we cultivated a bacterial community collected from biofilms in Kapova Cave (Shulgan–Tash Nature Reserve, Bashkortostan), and assessed its ability to synthesize secreted hydrolytic enzymes including RNases, proteases, and amylases.

Materials and Methods: Isolated bacteria were identified by V3-V4 16S rRNA region sequencing. Enzymatic activities were assessed by measuring transparency zones around colonies grown on the appropriate substrate (RNA, casein, starch). Functional profiles of the communitieswere predicted using the Global Mapper module on iVikodak. Taxonomic, structural, and compositional diversity were calculated using Shannon–Wiener and Bray–Curtis indices.

Results: Eighty-nine percent of 102 bacterial isolates were Proteobacteria, whereas other isolates were divided into three other phyla, Actinobacteria, Firmicutes, and Bacteroidetes that comprised 5%, 4%, and 2% of the isolates, respectively. Genus Pseudomonas was predominant with 42 isolates. Six isolates showed no extracellular enzymatic activity at all, 73 isolates expressed protease, 57 isolates expressed amylase, and 71 isolates had RNase activity. All three extracellular enzymes were expressed by 39isolates.

Conclusion: The biodiversity of cultivated microbiota from Kapova Cave was characterized. Bacteria that produce large amounts of protease, RNase and amylase were identified as Stenotrophomonas rhizophila, Lysinibacillus fusiformis, and Pseudomonas stutzeri, respectively.

Supporting Institution

Russian Science Foundation

Project Number

No 22-24-00036.

Thanks

We thank the colleagues working within the framework of Program “Priority-2030” for biofilm sampling.

References

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Year 2023, , 186 - 195, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1349885

Abstract

Project Number

No 22-24-00036.

References

  • Ortiz M, Legatzki A, Neilson J W, et al. Making a living while starving in the dark: metagenomic insights into the energy dy-namics of a carbonate cave. ISME J. 2014;8(2):478-491. google scholar
  • Zada S, Sajjad W, Rafiq M, et al. Cave microbes as a potential source of drugs development in the modern era. Microb Ecol. 2022;84:676-687. google scholar
  • Ahamada Rachid N, Doğruöz Güngör N. Major impacts of caving activities on cave microbial diversity: case study of Morca Cave, Turkey. Int Microbiol. 2023;26(2):179-190. google scholar
  • Adetutu EM, Ball AS. Microbial diversity and activity in caves. Microb Australia. 2014;35(4):192-194. google scholar
  • Abdullin SR, Kapralov SA, Kuzmina Y. Biota of the cave Shulgan-Tash (Kapova), State reserve “Shulgan-Tash”; 2012. ISBN 5904555415, 9785904555412. (in Russian). google scholar
  • Kuzmina LY, Galimzyanova NF, Chervyatsova OY, Sailfullina NM, Kapralov SA, Ryabova AS. Biogenous fouling in Shulgan-Tash cave (Kapova, Southern Urals) and factors influencing on their expansion. Ecobiotekh. 2019;2(2):128-142. google scholar
  • Galimzianova NF, Gilvanova EA, Ryabova AS, Guvatova ZG, Kudryavtseva AV, Melentiev AI. Phylogenetic diversity of prokaryotes in microbial communities inhabiting rock surfaces of Shulgan-Tash (Kapova) cave, Southern Urals. Ecobiotekh. 2020;3(3):298-304. google scholar
  • Wang Y, Cheng X, Wang H, Zhou J, Liu X, Tuovinen OH. The characterization of microbiome and interactions on weathered rocks in a subsurface karst cave, Central China. Front Microbiol. 2022;13:909494. doi:org/10.3389/fmicb.2022.909494. google scholar
  • Zhu HZ, Zhang ZF, Zhou N, et al. Bacteria and metabolic poten-tial in karst caves revealed by intensive bacterial cultivation and genome assembly. Appl Environ Microbiol. 2021;87(6):e02440-20. doi.org/10.1128/AEM.02440-20. google scholar
  • Cheng XY, Liu XY, Wang HM, et al. USC dominated community composition and cooccurrence network of methanotrophs and bacteria in subterranean karst caves, Microbiol Spectr. 2021;9(1): e0082021. doi:org/10.1128/Spectrum.00820-21. google scholar
  • Gulecal-Pektas Y. Bacterial diversity and composition in Oylat cave (Turkey) with combined Sanger/pyrosequencing approach. Pol J Microbiol. 2016;65(1):69-75. google scholar
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  • Razzaq A, Shamsi S, Ali A, et al. Microbial pro-teases applications. Front Bioeng Biotechnol. 2019;7:110. doi:org/10.3389/fbioe.2019.00110. google scholar
  • Rao RR, Vimudha M, Kamini N, Gowthaman M, Chan-drasekran B, Saravanan P. Alkaline protease production from Brevibacterium luteolum (MTCC 5982) under solid-state fermen-tation and its application for sulfide-free unhairing of cowhides. Appl Biochem Biotechnol. 2017;182:511-528 google scholar
  • De Souza PM, de Oliveira e Magalhâes P. Application of mi-crobial a-amylase in industry - A review. Braz J Microbiol. 2010;41(4):850-861. google scholar
  • Gopinath SC, Anbu P, Arshad MK, et al. Biotechnological processes in microbial amylase production. Biomed Res Int. 2017:1272193. doi:org/10.1155/2017/1272193. google scholar
  • Shah Mahmud R, Efimova MA, Ulyanova V. et al. Bacillus pumilus ribonuclease rescues mice infected by double-stranded RNA-containing reovirus serotype 1. Virus Res. 2020;286:198086. doi:10.1016/j.virusres.2020.198086. google scholar
  • Shah Mahmud R, Mostafa A, Müller C, et al. Bacterial ribonu-clease binase exerts an intra-cellular anti-viral mode of action tar-geting viral RNAs in influenza a virus-infected MDCK-II cells. Virol J. 2018;15(1):5. doi:org/10.1186/s12985-017-0915-1. google scholar
  • Shah Mahmud R, Müller C, Romanova Y, et al. Ribonuclease from Bacillus acts as an antiviral agent against negative- and positive-sense single stranded human respiratory RNA. Viruses Biomed Res Int. 2017:5279065. doi:org/10.1155/2017/5279065, 2017. google scholar
  • Shah Mahmud R, Efimova M, Mostafa A, Ulyanova V, Ilin-skaya O. Antiviral activity of bacterial extracellular ribonucle-ase against single-, double-stranded RNA and DNA containing viruses in cell cultures. BioNanoSci. 2016;6:561-563. google scholar
  • Mitkevich VA, Pace CN, Koschinski A, Makarov AA, Ilinskaya ON. Cytotoxicity mechanism of the RNase Sa cationic mutants involves inhibition of potassium current through Ca2+ -activated channels. Mol Biol. 2015;49:933-938. google scholar
  • Ilinskaya ON, Shah-Mahmud RS. Ribonucleases as antiviral agents. Mol Biol. 2014;48(5):615-623. google scholar
  • Khodzhaeva V, Makeeva A, Ulyanova V, et al. Binase immobilized on halloysite nanotubes exerts enhanced cytotoxicity toward hu-man colon adenocarcinoma cells. Front Pharmacol. 2017;8:631. doi:org/10.3389/fphar.2017.00631. google scholar
  • Walters W, Hyde ER, Berg-Lyons D, et al. Improved bacterial 16S rRNA gene (v4 and v4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems. 2016;1(1):e00009-15. doi:10.1128/mSystems.00009-15. google scholar
  • Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: A better web interface. Nucleic Acids Res. 2008;36:W5-9. doi:10.1093/nar/gkn201 google scholar
  • . Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547-1549. google scholar
  • Jeffris GD, Holtman WF, Guse D. Rapid method for determin-ing the activity of microorganisms on nucleic acids. J Bacteriol. 1957;73:591-601. google scholar
  • Price MF, Wilkinson ID, Gentry LO. Plate method for detec-tion of phospholipase activity in Candida albicans. Sabouraudia. 1982;20(1):7-14. google scholar
  • Nagpal S, Haque MM, Singh R, Mande SS. iVikodak - A platform and standard workflow for inferring, analyzing, comparing, and visualizing the functional potential of microbial communities, Front Microbial. 2019;9:1-15. google scholar
  • Bray JR, Curtis JT. An ordination of the upland forest communities of Southern Wisconsin. Ecological Monographs. 1957;27:325-349. google scholar
  • Klinfoong R, Thummakasorn C, Ungwiwatkul S, BOONTANOM P, Chantarasirid A. Diversity and activity of amylase-producing bacteria isolated from mangrove soil in Thailand. Biodiversitas 2022;23(10):5519-5531. doi:10.13057/biodiv/d231064. google scholar
  • Khannous L, Jrad M, Dammak M, et al. Isolation of a novel amylase and lipase-producing Pseudomonas luteola strain: Study of amylase production conditions. Lipids Health Dis. 2014;13:9. doi:10.1186/1476-511X-13-9. google scholar
  • Xu C, Zhao L, Du W, Zhang S, Wu Y, Zhou F. Food sources and trophic levels of terrestrial cave fauna in Yuping Town, Libo County, Guizhou Province. Biodiv Sci. 2021;29(8): 1108-1119. google scholar
  • Fu L, Monro AK, Wei Y. Cataloguing vascular plant diver-sity of karst caves in China. Biodiv Sci. 2022;30(7):21537. doi:org/10.17520/biods.2021537. google scholar
  • Liu R, Zhang Z, Shen J, Wang Z. Community characteristics of bryophyte in Karst caves and its effect on heavy metal pollu-tion: A case study of Zhijin Cave, Guizhou Province, Biodiv Sci. 2018;26(12):1277-1288. google scholar
  • Nazik L, Poyraz M, Karabiyikoglu M. Karstic Landscapes and Landforms in Turkey. In book: Landscapes and Land-forms of Turkey. Chapter: 5. Springer Nature; 2019:181-196. doi:10.1007/978-3-030-03515-0_5. google scholar
  • Gao C, Guo L. Progress on microbial species diver-sity, community assembly and functional traits. Biodiv Sci. 2022;30(10):22429. doi:org/10.17520/biods.2022429. google scholar
  • Chelius MK, Beresford G, Horton H, et al. Impacts of alterations of organic inputs on the bacterial community within the sediments of wind cave, South Dakota, USA. Int J Speleol.2009:38(1):1-10. doi:10.5038/1827-806X.38.1.1. google scholar
  • Holmes AJ, Tujula NA, Holley M, et al. Phylogenetic structure of unusual aquatic microbial formations in Nullarbor caves, Aus-tralia. Environ Microbiol. 2001;3(4):256-264. google scholar
  • Macalady JL, Jones DS, Lyon EH. Extremely acidic, pendulous cave wall biofilms from the Frasassi cave system, Italy. Environ Microbiol. 2007;9(6):1402-1414. google scholar
  • Schabereiter-Gurtner C, Saiz-Jimenez C, Pinar G, Lubitz W, Rölleke S. Phylogenetic diversity of bacteria associated with Pale-olithic paintings and surrounding rock walls in two Spanish caves (Llonm and La Garma). FEMS Microbiol Ecol. 2004;47(2):235-247. google scholar
  • Zhou JP, Gu YQ, Zou CS, Mo MH. Phylogenetic diversity of bacteria in an earth-cave in Guizhou province, southwest of China. J Microbiol. 2007;45(2):105-112. google scholar
  • Gonzalez JM, Portillo MC, Saiz-Jimenez C. Metabolically active crenarchaeota in Altamira Cave. Naturwissenschaften. 2006;93(1):42-45. google scholar
  • Leuko S, Koskinen K, Sanna L, et al. The influence of human exploration on the microbial community structure and ammonia oxidizing potential of the Su Bentu lime-stone cave in Sardinia, Italy. PLoS One. 2017;12(7):e0180700. doi:org/10.1371/journal.pone.0180700. google scholar
  • Doğruöz-Güngör N, Arslan-Aydoğdu EÖ, Dirmit E, Usuloğlu E. Anthropogenic impacts on the bacterial profile of Yarik Sinkhole in Antalya, Turkey. J Caves Karst Stud. 2020;82(2):116-124. google scholar
  • Yücel S, Yamaç M. Selection of Streptomyces isolates from Turkish karstic caves against antibiotic resistant microorganisms. Pak J Pharm Sci. 2010;23(1):1-6. google scholar
  • Rusznyak A, Akob DM, Nietzsche S, et al. Calcite biomin-eralization by bacterial isolates from the recently discov-ered pristine karstic herrenberg cave, Appl Environ Microbiol. 2012;78(4):1157-1167. google scholar
  • Cuzman OA, Luvidi L, Colantonio C, et al. Biodiversity and conservation correlation in the case of a Roman fresco located in a semi-confined environment. Int Biodet Biodeg. 2023;181:105605. doi.org/10.1016/j.ibiod.2023.105605. google scholar
  • Pinski A, Zur J, Hasterok R, Hupert-Kocurek K. Comparative ge-nomics of Stenotrophomonas maltophilia and Stenotrophomonas rhizophila revealed characteristic features of both species. Int J Mol Sci. 2020;21(14):4922. doi:org/10.3390/jms21144922. google scholar
  • Ahmed I, Yokota A, Yamazoe A, Fujiwara T. Proposal of Lysini-bacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. Int J Syst Evol Microbiol. 2007;5:1117-1125. google scholar
  • Kan Y, Niu XK, Rao MPN, et al. Lysinibacillus cavernae sp. nov., isolated from cave soil. Arch Microbiol. 2020;202(6):1529-1534. google scholar
  • Narsing Rao MP, Dong Z.Y, Niu XK, et al. Lysinibacillus antri sp. nov., isolated from cave soil. Int J Syst Evol Microbiol. 2020;70(5):3295-3299. google scholar
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There are 58 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Articles
Authors

William Kurdy 0009-0005-9405-3019

Galina Yakovleva 0000-0002-8504-3434

Olga Ilinskaya 0000-0001-6936-2032

Project Number No 22-24-00036.
Publication Date December 21, 2023
Submission Date August 25, 2023
Published in Issue Year 2023

Cite

AMA Kurdy W, Yakovleva G, Ilinskaya O. Bacterial Biodiversity of the Kapova Karst Cave as a Source of Hydrolases Producers. Eur J Biol. December 2023;82(2):186-195. doi:10.26650/EurJBiol.2023.1349885