Skip to main content

Advertisement

SpringerLink
Log in

Composition and functional profiles of microbial communities in two geochemically and mineralogically different caves

  • Environmental Biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Microbial communities in cave ecosystems have specific survival strategies, which is far from being well explicated. Here, we reported the genetic and functional diversity of bacteria and archaea in typical limestone (Kashmir Cave) and silicate-containing (Tiser Cave) caves. X-ray diffraction (XRD) and Fourier transform infrared spectroscopic (FTIR) analyses revealed the different geochemical and mineral compositions of the two caves. Amplicon barcode sequencing revealed the dominancy of Actinobacteria and Proteobacteria in Kashmir and Tiser Caves. Bacteroidetes and Firmicutes were the dominant phyla in Tiser Cave, and the abundance is relatively small in Kashmir Cave. Archaea was also abundant prokaryotes in Kashmir Cave, but it only accounted for 0.723% of the total prokaryote sequences in Tiser Cave. Functional analysis based on metagenomic sequencing data revealed that a large number of functional potential genes involved in nutrient metabolism and biosynthesis of bioactive compounds in Tiser and Kashmir Cave samples could significantly influence the biogeochemical cycle and secondary metabolite production in cave habitats. In addition, the two caves were also found to be rich in biosynthetic genes, encoding bioactive compounds, such as monobactam and prodigiosin, indicating that these caves could be potential habitats for the isolation of antibiotics. This study provides a comprehensive insight into the diversity of bacteria and archaea in cave ecosystems and helps to better understand the special survival strategies of microorganisms in cave ecosystems.

Key points

• Geochemically distinct caves possess unique microbial community structure.

• Cavernicoles could be important candidates for antibiotic production.

• Cavernicoles are important for biogeochemical cycling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

16S rRNA gene sequencing data and metagenomic shotgun sequencing data are available in the NCBI Sequence Read Archive (SRA) (http://www.ncbi.nlm.nih.gov/sra) with the accession number of PRJNA741692 and PRJNA741999, respectively.

References

  • Adetutu EM, Ball AS (2014) Microbial diversity and activity in caves. Microbiol Aust 35:192–194

    Article  Google Scholar 

  • Adetutu EM, Thorpe K, Bourne S, Cao X, Shahsavari E, Kirby G, Ball AS (2011) Phylogenetic diversity of fungal communities in areas accessible and not accessible to tourists in Naracoorte Caves. Mycologia 103:959–968

    Article  PubMed  Google Scholar 

  • Adetutu EM, Thorpe K, Shahsavari E, Bourne S, Cao X, Fard RMN, Kirby G, Ball AS (2012) Bacterial community survey of sediments at Naracoorte Caves, Australia. Int J Speleol 41:137–147

    Article  Google Scholar 

  • Alkhalili RN, Bernfur K, Dishisha T, Mamo G, Schelin J, Canbäck B, Emanuelsson C, Hatti-Kaul R (2016) Antimicrobial protein candidates from the Thermophilic Geobacillus sp. strain ZGt-1: production, proteomics, and bioinformatics analysis. Int J Mol Sci 17:1363

    Article  PubMed Central  Google Scholar 

  • Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8:251–259

    Article  PubMed  CAS  Google Scholar 

  • Anandan R, Dharumadurai D, Manogaran GP (2016) An introduction to Actinobacteria. In: Actinobacteria-Basics and Biotechnological Applications. Intechopen. 3–37.

  • Awais M, Pervez A, Yaqub A, Shah MM (2010) Production of antimicrobial metabolites by Bacillus subtilis immobilized in polyacrylamide gel. Pak J Zool 42:267–275

    CAS  Google Scholar 

  • Axenov-Gibanov DV, Voytsekhovskaya IV, Tokovenko BT, Protasov ES, Gamaiunov SV, Rebets YV, Luzhetskyy AN, Timofeyev MA (2016) Actinobacteria isolated from an underground lake and moonmilk speleothem from the biggest conglomeratic karstic cave in Siberia as sources of novel biologically active compounds. PLoS One 11:e0149216

    Article  PubMed  PubMed Central  Google Scholar 

  • Balkwill DL, Drake GR, Reeves RH, Fredrickson JK, White DC, Ringelberg DB, Chandler DP, Romine MF, Kennedy DW, Spadoni CM (1997) Taxonomic study of aromatic-degrading bacteria from deep terrestrial subsurface sediments and description of Sphingomonas aromaticivorans sp. nov., Sphingomonas subterranea sp. nov., and Sphingomonas stygia sp. nov. Int J Syst Evol Microbiol 47:191–201

    CAS  Google Scholar 

  • Banat IM, Franzetti A, Martinotti M, Fracchia L (2010) Microbial biosurfactants production, applications and future potential. Appl Microbiol Biotechnol 87:427–444

    Article  PubMed  CAS  Google Scholar 

  • Barton HA (2006) Introduction to cave microbiology : a review for the non-specialist. J Cave Karst Stud 68:43–54

    Google Scholar 

  • Barton HA, Jurado V (2007) What’s up down there? Microbial diversity in caves microorganisms in caves survive under nutrient poor conditions and are metabolically versatile and unexpectedly diverse. Artic Microbe (washington, DC) 2:132–138

    Google Scholar 

  • Belyagoubi L, Belyagoubi-Benhammou N, Jurado V, Dupont J, Lacoste S, Djebbah F, Fatima O, Souad B, Salim H, Djamel A, Cesareo S-J (2018) Antimicrobial activities of culturable microorganisms (Actinomycetes and fungi) isolated from Chaabe Cave, Algeria. Int J Speleol 47:189–199

    Article  Google Scholar 

  • Bhardwaj A, Chaman S, Verma S (2017) Production of antibacterial agent from fungi isolated from pharmaceutical soil sample by fermentation under optimized conditions. Asian J Pharm Clin Res 10:110–115

    Article  CAS  Google Scholar 

  • Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG (2018) Optimizing taxonomic classification of marker gene amplicon sequences. PeerJ Prepr 6:e3208v2

    Google Scholar 

  • Brock TD, Madigan MT, Martinko JM, Parker J (2003) Brock biology of microorganisms. Prentice-Hall, Upper Saddle River (NJ)

    Google Scholar 

  • Candiroğlu B, Doğruöz Güngör N (2020) The biotechnological potentials of bacteria isolated from Parsık Cave, Turkey. Johnson Matthey Technol Rev 64:466

    Article  Google Scholar 

  • Cañveras JC, Sanchez-Moral S, Sloer V, Saiz-Jimenez C (2001) Microorganisms and microbially induced fabrics in cave walls. Geomicrobiol J 18:223–240

    Article  Google Scholar 

  • Cantillo A, Shapiro N, Woyke T, Kyrpides NC, Baena S, Zambrano MM (2018) Genome sequences of Actinobacteria from extreme environments in Colombia. Microbiol Resour Announc 7:e01384-e1418

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen M, Xu P, Zeng G, Yang C, Huang D, Zhang J (2015) Bioremediation of soils contaminated with polycyclic aromatic hydrocarbons, petroleum, pesticides, chlorophenols and heavy metals by composting: applications, microbes and future research needs. Biotechnol Adv 33:745–755

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Wu L, Boden R, Hillebrand-Voiculescu A, Kumaresan D, Moussard H, Baciu M, Lu Y, Colin Murrell J (2009) Life without light: microbial diversity and evidence of sulfur and ammonium based chemolithotrophy in Movile Cave. ISME J 3:1093–1104

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Herting CJ, Ross JL, Gabanic B, Puigdelloses-Vallcorba M, Szulzewsky F, Wojciechowicz ML, Cimino PJ, Ezhilarasan R, Sulman EP (2020) Genetic driver mutations introduced in identical cell of origin in murine glioblastoma reveal distinct immune landscapes but similar response to checkpoint blockade. Glia 68:2148–2166

    Article  PubMed  PubMed Central  Google Scholar 

  • Cockell CS, Kelly LC, Marteinsson V (2013) Actinobacteria—an ancient phylum active in volcanic rock weathering. Geomicrobiol J 30:706–720

    Article  CAS  Google Scholar 

  • Cuezva S, Fernandez-Cortes A, Porca E, Pasic L, Jurado V, Hernandez-Marine M, Serrano-Ortiz P, Hermosin B, Canaveras JC, Sanchez-Moral S, Saiz-Jimenez C (2012) The biogeochemical role of Actinobacteria in Altamira Cave, Spain. FEMS Microbiol Ecol 81:281–290

    Article  PubMed  CAS  Google Scholar 

  • Davidson MM, Silver BJ, Onstott TC, Moser DP, Gihring TM, Pratt LM, Boice EA, Lollar BS, Lippmann-Pipke J, Pfiffner SM (2011) Capture of planktonic microbial diversity in fractures by long term monitoring of flowing boreholes, Evander Basin, South Africa. Geomicrobiol J 28:275–300

    Article  Google Scholar 

  • Davis MC, Garey JR (2018) Microbial function and hydrochemistry within a stratified anchialine sinkhole: a window into coastal aquifer interactions. Water 10:972

    Article  Google Scholar 

  • De Mandal S, Chatterjee R, Kumar NS (2017) Dominant bacterial phyla in caves and their predicted functional roles in C and N cycle. BMC Microbiol 17:1–9

    Article  Google Scholar 

  • Desai MS, Assig K, Dattagupta S (2013) Nitrogen fixation in distinct microbial niches within a chemoautotrophy driven cave ecosystem. ISME J 7:2411–2423

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dhami NK, Reddy MS, Mukherjee A (2014) Application of calcifying bacteria for remediation of stones and cultural heritages. Front Microbiol 5:137–164

    Article  Google Scholar 

  • Dong Y, Kumar CG, Chia N, Kim P, Miller PA, Price ND, Cann IKO, Flynn TM, Sanford RA, Krapac IG (2014) Halomonas sulfidaeris dominated microbial community inhabits a 1.8 km-deep subsurface Cambrian sandstone reservoir. Environ Microbiol 16:1695–1708

    Article  PubMed  CAS  Google Scholar 

  • Engel AS, Gupta AA (2014) Regime shift in sandy beach microbial communities following deepwater horizon oil spill remediation efforts. PLoS One 9:e102934

    Article  PubMed  PubMed Central  Google Scholar 

  • Engel AS, Meisinger DB, Porter ML, Payn RA, Schmid M, Stern LA, Schleifer KH, Lee NM (2009) Linking phylogenetic and functional diversity to nutrient spiraling in microbial mats from Lower Kane Cave ( USA ). ISME J 4:98–110

    Article  PubMed  CAS  Google Scholar 

  • Genilloud O (2017) Actinomycetes: still a source of novel antibiotics. Nat Prod Rep 34:1203–1232

    Article  PubMed  CAS  Google Scholar 

  • Ghrairi T, Ben BO, Hani K (2015) Detection and characterization of a bacteriocin, putadicin T01, produced by Pseudomonas putida isolated from hot spring water. APMIS 123:260–268

    Article  PubMed  CAS  Google Scholar 

  • Gillieson D (1996) Caves: processes, development management. Blackwell, Oxford

    Book  Google Scholar 

  • Gosse JT, Ghosh S, Sproule A, Overy D, Cheeptham N, Boddy CN (2019) Whole genome sequencing and metabolomic study of cave Streptomyces isolates ICC1 and ICC4. Front Microbiol 10:1020

    Article  PubMed  PubMed Central  Google Scholar 

  • Gramain A, Díaz GC, Demergasso C, Lowenstein TK, McGenity TJ (2011) Archaeal diversity along a subterranean salt core from the Salar Grande (Chile). Environ Microbiol 13:2105–2121

    Article  PubMed  Google Scholar 

  • Hall M, Beiko RG (2018) 16S rRNA gene analysis with QIIME2. In: Microbiome analysis. Springer 113–129

  • Hartmann R, Sickinger H-D, Oesterhelt D (1980) Anaerobic growth of Halobacteria. Proc Natl Acad Sci 77:3821–3825

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holmes AJ, Tujula NA, Holley M, Contos A, James JM, Rogers P, Gillings MR (2001) Phylogenetic structure of unusual aquatic microbial formations in Nullarbor caves, Australia. Environ Microbiol 3:256–264

    Article  PubMed  CAS  Google Scholar 

  • Hussein EI, Jacob JH, Shakhatreh MAK, Abd Al-Razaq MA, Juhmani A-SF, Cornelison CT (2018) Detection of antibiotic producing Actinobacteria in the sediment and water of Ma’in thermal springs (Jordan). Germs 8:191–198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Idris H, Goodfellow M, Sanderson R, Asenjo JA, Bull AT (2017) Actinobacterial rare biospheres and dark matter revealed in habitats of the Chilean Atacama Desert. Sci Rep 7:1–11

    Article  Google Scholar 

  • Jaffe R, Prous X, Zampaulo R, Giannini TC, Imperatriz-Fonseca VL, Maurity C, Oliveira G, Brandi IV, Siqueira JO (2016) Reconciling mining with the conservation of cave biodiversity: a quantitative baseline to help establish conservation priorities. PLoS One 11:e0168348

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang Z, Guo L, Chen C, Liu S, Zhang L, Dai S, He Q, You X, Hu X, Tuo L, Jiang W, Sun C (2015) Xiakemycin A, a novel pyranonaphthoquinone antibiotic, produced by the Streptomyces sp. CC8-201 from the soil of a karst cave. J Antibiot (tokyo) 68:771–774

    Article  CAS  Google Scholar 

  • Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731

    Article  PubMed  CAS  Google Scholar 

  • Kelly DP, Wood AP (1994) Enzymes involved in microbiological oxidation of thiosulfate and polythionates. Methods Enzymol 243:501–510

    Article  CAS  Google Scholar 

  • Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the Proteobacteria. In: The prokaryotes: a handbook on the biology of bacteria, Springer 3–37

  • Kieser S, Brown J, Zdobnov EM, Trajkovski M, McCue LA (2020) ATLAS: a Snakemake workflow for assembly, annotation, and genomic binning of metagenome sequence data. BMC Bioinformatics 21:1–8

    Article  Google Scholar 

  • Kim BS, Lee JY, Hwang BK (1998) Diversity of Actinomycetes antagonistic to plant pathogenic fungi in cave and sea-mud soils of Korea. J Microbiol 36:86–92

    Google Scholar 

  • Kumbhare SV, Dhotre DP, Dhar SK, Jani K, Apte DA, Shouche YS, Sharma A (2015) Insights into diversity and imputed metabolic potential of bacterial communities in the continental shelf of Agatti Island. PLoS One 10:e0129864

    Article  PubMed  PubMed Central  Google Scholar 

  • Le-Roy N, Jackson DJ, Marie B, Ramos-Silva P, Marin F (2015) Carbonic anhydrase and metazoan biocalcification: a focus on molluscs Key Engineering Materials. Trans Tech Publ 672:151–157

    Google Scholar 

  • Li D, Liu C-M, Luo R, Sadakane K, Lam T-W (2015) MEGAHIT: an ultra fast single node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31:1674–1676

    Article  PubMed  CAS  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  CAS  PubMed  Google Scholar 

  • Luncini G, Demain AL (2009) Secondary metabolism in bacteria: antibiotic pathways, regulation, and function. Biol prokaryotes Blackwell Sci Ltd 627–651

  • Ma HK, Liu MM, Li SY, Wu Q, Chen JC, Chen GQ (2013) Application of polyhydroxyalkanoate (PHA) synthesis regulatory protein PhaR as a bio-surfactant and bactericidal agent. J Biotechnol 166:34–41

    Article  PubMed  CAS  Google Scholar 

  • Maciejewska M, Adam D, Martinet L, Naômé A, Całusińska M, Delfosse P, Carnol M, Barton HA, Hayette M-P, Smargiasso N (2016) A phenotypic and genotypic analysis of the antimicrobial potential of cultivable Streptomyces isolated from cave moonmilk deposits. Front Microbiol 7:1455

    Article  PubMed  PubMed Central  Google Scholar 

  • Maciejewska M, Całusińska M, Cornet L, Adam D, Pessi IS, Malchair S, Delfosse P, Baurain D, Barton HA, Carnol M (2018) High-throughput sequencing analysis of the Actinobacterial spatial diversity in moonmilk deposits. Antibiotics 7:27

    Article  PubMed Central  Google Scholar 

  • Madigan MT, Martinko JM, Parker J (1997) Brock biology of microorganisms. Prentice hall, Upper Saddle River NJ

    Google Scholar 

  • Monciardini P, Iorio M, Maffioli S, Sosio M, Donadio S (2014) Discovering new bioactive molecules from microbial sources. Microb Biotechnol 7:209–220

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muhammad SA, Ahmad S, Hameed A (2009) Antibiotic production by thermophilic Bacillus specie SAT-4. Pak J Pharm Sci 22:339–345

    PubMed  CAS  Google Scholar 

  • Norris PR, Davis-Belmar CS, Brown CF, Calvo-Bado LA (2011) Autotrophic, sulfur-oxidizing Actinobacteria in acidic environments. Extremophiles 15:155–163

    Article  PubMed  CAS  Google Scholar 

  • Northup DE, Lavoie KH (2001) Geomicrobiology of Caves: A Review. Geomicrobiol J 18:199–222

  • Northup DE, Melim LA, Spilde MN, Hathaway JJM, Garcia MG, Moya M, Stone FD, Boston PJ, Dapkevicius M, Riquelme C (2011) Lava cave microbial communities within mats and secondary mineral deposits: implications for life detection on other planets. Astrobiology 11:601–618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens, MHH, Wagner H (2018) Community Ecology Package. R package version 2.5–1

  • Oliveira C, Gunderman L, Coles CA, Lochmann J, Parks M, Ballard E, Glazko G, Rahmatallah Y, Tackett AJ, Thomas DJ (2017) 16S rRNA gene-based metagenomic analysis of Ozark cave bacteria. Diversity 9:31

    Article  PubMed  PubMed Central  Google Scholar 

  • Oren A, Litchfield CD (1999) A procedure for the enrichment and isolation of Halobacterium. FEMS Microbiol Lett 173:353–358

    Article  CAS  Google Scholar 

  • Ortiz M, Neilson JW, Nelson WM, Legatzki A, Byrne A, Yu Y, Wing RA, Soderlund CA, Pryor BM, Pierson LS (2013) Profiling bacterial diversity and taxonomic composition on speleothem surfaces in Kartchner Caverns, AZ. Microb Ecol 65:371–383

    Article  PubMed  Google Scholar 

  • Palaniyandi SA, Yang SH, Damodharan K, Suh J (2013) Genetic and functional characterization of culturable plant-beneficial Actinobacteria associated with yam rhizosphere. J Basic Microbiol 53:985–995

    Article  Google Scholar 

  • Pakes MJ (2013) Anchialine cave environments: a novel chemosynthetic ecosystem and its ecology. UC Berkeley Electronic Theses and Dissertations.

  • Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods 14:417–419

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paun VI, Lavin P, Chifiriuc MC, Purcarea C (2021) First report on antibiotic resistance and antimicrobial activity of bacterial isolates from 13,000-year old cave ice core. Sci Rep 11:1–15

    Article  Google Scholar 

  • Pester M, Maixner F, Berry D, Rattei T, Koch H, Lücker S, Nowka B, Richter A, Spieck E, Lebedeva E (2014) NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ Microbiol 16:3055–3071

    Article  PubMed  CAS  Google Scholar 

  • Pipan T, Deharveng L, Culver DC (2020) Hotspots of Subterranean Biodiversity. Diversity 12:209

    Article  Google Scholar 

  • Podgorsek L, Imhoff JF (1999) Tetrathionate production by sulfur oxidizing bacteria and the role of tetrathionate in the sulfur cycle of Baltic Sea sediments. Aquat Microb Ecol 17:255–265

    Article  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  CAS  PubMed  Google Scholar 

  • Rangseekaew P, Pathom-aree W (2019) Cave Actinobacteria as producers of bioactive metabolites. Front Microbiol 10:387

    Article  PubMed  PubMed Central  Google Scholar 

  • Rateb ME, Houssen WE, Harrison WTA, Deng H, Okoro CK, Asenjo JA, Andrews BA, Bull AT, Goodfellow M, Ebel R (2011) Diverse metabolic profiles of a Streptomyces strain isolated from a hyper-arid environment. J Nat Prod 74:1965–1971

    Article  PubMed  CAS  Google Scholar 

  • Riquelme C, de Dapkevicius ML, Miller AZ, Charlop-Powers Z, Brady S, Mason C, Cheeptham N (2017) Biotechnological potential of Actinobacteria from Canadian and Azorean volcanic caves. Appl Microbiol Biotechnol 101:843–857

    Article  PubMed  CAS  Google Scholar 

  • Rule D, Cheeptham N (2013) The effects of UV light on the antimicrobial activities of cave Actinomycetes. Int J Speleol 42:147–153

    Article  Google Scholar 

  • Saiz-Jimenez C (2012) Microbiological and environmental issues in show caves. World J Microbiol Biotechnol 28:2453–2464

    Article  PubMed  Google Scholar 

  • Sajjad W, Khan S, Ahmad M, Rafiq M, Badshah M, Sajjad W, Zada S, Khan S, Hasan F, Shah AA (2018a) Effects of ultra-violet radiation on cellular proteins and lipids of radioresistant bacteria isolated from desert soil. Folia Biol 66:41–52

    Article  CAS  Google Scholar 

  • Sajjad W, Zheng G, Zhang G, Ma X, Xu W, Ali B, Rafiq M (2018b) Diversity of prokaryotic communities indigenous to acid mine drainage and related rocks from Baiyin Open-Pit Copper Mine Stope, China. Geomicrobiol J 35:580–600

    Article  Google Scholar 

  • Sánchez LA, Gómez FF, Delgado OD (2009) Cold-adapted microorganisms as a source of new antimicrobials. Extremophiles 13:111–120

    Article  PubMed  Google Scholar 

  • Sajjad W, Zheng G, Ma X, Rafiq M, Irfan M, Xu W, Ali B (2019) Culture-dependent hunt and characterization of iron-oxidizing bacteria in Baiyin Copper Mine, China and their application in metals extraction. J Basic Microbiol 59:323–336

  • Sand W (1997) Microbial mechanisms of deterioration of inorganic substrates—a general mechanistic overview. Int Biodeterior Biodegradation 40:183–190

    Article  CAS  Google Scholar 

  • Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272:1953–1955

    Article  PubMed  CAS  Google Scholar 

  • Sarmiento-Vizcaíno A, Braña AF, Pérez-Victoria I, Martín J, De Pedro N, Cruz MD, Díaz C, Vicente F, Acuña JL, Reyes F (2017) Paulomycin g, a new natural product with cytotoxic activity against tumor cell lines produced by deep-sea sediment derived Micromonospora matsumotoense M-412 from the Avilés canyon in the Cantabrian Sea. Mar Drugs 15:271

    Article  PubMed Central  Google Scholar 

  • Sathya A, Vijayabharathi R, Gopalakrishnan S (2017) Plant growth promoting Actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3Biotech 7:1–10

    Google Scholar 

  • Schluter D (1996) Ecological causes of adaptive radiation. Am Nat 148:S40–S64

    Article  Google Scholar 

  • Schubert BA, Lowenstein TK, Timofeeff MN, Parker MA (2010) Halophilic archaea cultured from ancient halite, Death Valley, California. Environ Microbiol 12:440–454

    Article  PubMed  CAS  Google Scholar 

  • Searle MP (2011) Geological evolution of the Karakoram Ranges. Ital J Geosci 130:147–159

    Google Scholar 

  • Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069

    Article  CAS  PubMed  Google Scholar 

  • Shivlata L, Tulasi S (2015) Thermophilic and alkaliphilic Actinobacteria: biology and potential applications. Front Microbiol 6:1014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sievert SM, Kiene RP, Schulz-Vogt HN (2007) The sulfur cycle. Oceanography 20:117–123

    Article  Google Scholar 

  • Simon KS (2019) Cave ecosystems. In: Encyclopedia of caves. Elsevier 223–226

  • Singh G, Bhalla A, Ralhan PK (2011) Extremophiles and extremozymes: importance in current biotechnology. Int J Bioflux Soc 3:46–54

    CAS  Google Scholar 

  • Singh O, Gabani P (2011) Extremophiles: radiation resistance microbial reserves and therapeutic implications. J Appl Microbiol 110:851–861

    Article  PubMed  CAS  Google Scholar 

  • Spain AM, Krumholz LR, Elshahed MS (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3:992–1000

    Article  PubMed  CAS  Google Scholar 

  • Stankovic N, Radulovic V, Petkovic M, Vuckovic I, Jadranin M, Vasiljevic B, Nikodinovic-Runic J (2012) Streptomyces sp. JS520 produces exceptionally high quantities of undecylprodigiosin with antibacterial, antioxidative, and UV-protective properties. Appl Microbiol Biotechnol 96:1217–1231

    Article  PubMed  CAS  Google Scholar 

  • Tempest DW, Meers JL, Brown CM (1970) Synthesis of glutamate in Aerobacter aerogenes by a hitherto unknown route. Biochem J 117:405–407

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tisato N, Torriani SFF, Monteux S, Sauro F, De Waele J, Tavagna ML, D’Angeli IM, Chailloux D, Renda M, Eglinton TI (2015) Microbial mediation of complex subterranean mineral structures. Sci Rep 5:1–10

    Article  Google Scholar 

  • Tiwari K, Gupta RK (2012) Rare Actinomycetes: a potential storehouse for novel antibiotics. Crit Rev Biotechnol 32:108–132

    Article  PubMed  CAS  Google Scholar 

  • Tomczyk-Żak K, Zielenkiewicz U (2016) Microbial diversity in caves. Geomicrobiol J 33:20–38

    Article  Google Scholar 

  • Tuo L, Guo L, Liu S-W, Liu J-M, Zhang Y-Q, Jiang Z-K, Liu X-F, Chen L, Zu J, Sun C-H (2015) Lysinibacter cavernae gen. nov., sp. nov., a new member of the family Microbacteriaceae isolated from a karst cave. Int J Syst Evol Microbiol 65:3305–3312

    Article  PubMed  CAS  Google Scholar 

  • Wang H, He Y, Liu W, Zhou A, Kolpakova M, Krivonogov S, Liu Z (2019) Lake water depth controlling archaeal tetraether distributions in midlatitude Asia: implications for paleo lake-level reconstruction. Geophys Res Lett 46:5274–5283

    Article  Google Scholar 

  • Ward AC, Allenby NEE (2018) Genome mining for the search and discovery of bioactive compounds: the Streptomyces paradigm. FEMS Microbiol Lett 365:fny240

    CAS  Google Scholar 

  • Wickham H Springer; New York, NY: 2009. Ggplot2 Elegant Graph Data Anal Sch

  • Williamson NR, Fineran PC, Gristwood T, Chawrai SR, Leeper FJ, Salmond GPC (2007) Anticancer and immunosuppressive properties of bacterial prodiginines. Future Microbiol 2:605–618

    Article  PubMed  CAS  Google Scholar 

  • Williamson NR, Fineran PC, Leeper FJ, Salmond GPC (2006) The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4:887–899

    Article  PubMed  CAS  Google Scholar 

  • Wiseschart A, Mhuanthong W, Thongkam P, Tangphatsornruang S, Chantasingh D, Pootanakit K (2018) Bacterial diversity and phylogenetic analysis of type II polyketide synthase gene from Manao-Pee Cave, Thailand. Geomicrobiol J 35:518–527

    Article  CAS  Google Scholar 

  • Youssef NH, Ashlock-Savage KN, Elshahed MS (2012) Phylogenetic diversities and community structure of members of the extremely halophilic archaea (order Halobacteriales) in multiple saline sediment habitats. Appl Environ Microbiol 78:1332–1344

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yücel S, Yamaç M (2010) Selection of Streptomyces isolates from Turkish karstic caves against antibiotic resistant microorganisms. Pak J Pharm Sci 23:1–6

    PubMed  Google Scholar 

  • Zada S, Naseem AA, Lee S-J, Rafiq M, Khan I, Shah AA, Hasan F (2016) Geochemical and mineralogical analysis of Kashmir Cave (SMAST), Buner, Pakistan, and isolation and characterization of bacteria having antibacterial activity. J Cave Karst Stud 78:94–109

    Article  CAS  Google Scholar 

  • Zopfi J, Ferdelman TG, Fossing H (2004) Distribution and fate of sulfur intermediates sulfite, tetrathionate, thiosulfate, and elemental sulfur in marine sediments, in Sulfur Biogeochemistry—Past and Present, Vol. 379, eds J. P. Amend, K. J. Edwards, and T. W. Lyons (Boulder, CO: Geological Society of America) 97–116

Download references

Funding

Funding for this study was provided by the National Natural Science Foundation of China (32070113) and Guangdong Science and Technology Department (2019ST023, 2019A1515011139).

Author information

Authors and Affiliations

  1. Department of Biology, College of Science, Guangdong Provincial Key Laboratory of Marine Biotechnology, Institute of Marine Sciences, Shantou University, Shantou, China

    Sahib Zada, Jianmin Xie, Min Yang, Xiaoyu Yang, Zhong Hu & Hui Wang

  2. State Key Laboratory of Cryospheric Science, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, 730000, China

    Wasim Sajjad

  3. Department of Microbiology, Faculty of Life Sciences and Informatics, Engineering and Management Sciences, Balochistan University of Information Technology, Quetta, Pakistan

    Muhammad Rafiq

  4. Department of Microbiology, Quaid-I-Azam University, Islamabad, Pakistan

    Fariha Hasan

Authors
  1. Sahib Zada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianmin Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoyu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wasim Sajjad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Muhammad Rafiq
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fariha Hasan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhong Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SZ, FH, ZH, and HW designated the experiment; SZ, JX, MY, XY and HW conducted the experiment and analyzed data; SZ, WS, MR wrote the first draft; HZ and HW reviewed and revised the manuscript.

Corresponding author

Correspondence to Hui Wang.

Ethics declarations

Ethics approval

This article does not contain any human and animal studies.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Sahib Zada, Jianmin Xie and Min Yang are contributed equally

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 913 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zada, S., Xie, J., Yang, M. et al. Composition and functional profiles of microbial communities in two geochemically and mineralogically different caves. Appl Microbiol Biotechnol 105, 8921–8936 (2021). https://doi.org/10.1007/s00253-021-11658-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-021-11658-4

Keywords

Search

Navigation