Abstract
Designing novel isolation methods could enhance the diversification of the available bacterial strains to biotechnology. In this study, the new ex situ and in situ cultivation methods are introduced for the isolation of actinobacteria. In the ex situ experiments, the soil suspension was spread on the isolation media located above some ordinary papers in immediate contact with the slurry of soil substrate and incubated for 16 weeks. The paper was wholly immersed in the cave soil for in situ cultivations, and the containers were buried under layers of soil in Hampoeil cave for 10 weeks. Fruit wrapping kraft coated paper, with 68.8% recovery of isolates, was a better choice in isolation of actinobacteria than other studied filter paper. Based on the molecular identification results, 19% of the isolates obtained from the in situ cultivation method had less than 98.5% similarity to known taxa of actinobacteria and potentially may represent new species. In contrast, in the standard cultivation method, 1.3% of the isolates had less than 98.5% similarity 16Sr RNA gene. This data shows that the introduced cultivation method is a promising technique for isolating less culturable or new actinobacteria.
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Data availability
The datasets used and analyzed during the present study are available from the corresponding author on request.
References
Almasi F, Mohammadipanah F, Adhami H et al (2018) Introduction of marine-derived Streptomyces sp. UTMC 1334 as a source of pyrrole derivatives with anti-acetylcholinesterase activity. J Appl Microbiol 125:1370–1382. https://doi.org/10.1111/jam.14043
Baral B, Akhgari A, Metsä-Ketelä M (2018) Activation of microbial secondary metabolic pathways: avenues and challenges. Synth Syst Biotechnol 3:163–178. https://doi.org/10.1016/j.synbio.2018.09.001
Bodor A, Bounedjoum N, Vincze GRE et al (2020) Challenges of unculturable bacteria: environmental perspectives. Rev Environ Sci Bio 19:1–22. https://doi.org/10.1007/s11157-020-09522-4
Chaudhary DK, Khulan A, Kim J (2019) Development of a novel cultivation technique for uncultured soil bacteria. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-019-43182-x
Cross KL, Campbell JH, Balachandran M et al (2019) Targeted isolation and cultivation of uncultivated bacteria by reverse genomics. Nat Biotechnol 37:1314–1321. https://doi.org/10.1038/s41587-019-0260-6
Dagnon KL, Thellen C, Ratto JA et al (2010) Physical and thermal analysis of the degradation of poly (3-hydroxybutyrate-co-4-hydroxybutyrate) coated paper in a constructed soil medium. J Polym Environ 18:510–522. https://doi.org/10.1007/s10924-010-0231-y
de la Torre BG, Albericio F (2020) The pharmaceutical industry in 2019. An analysis of FDA drug approvals from the perspective of molecules. Molecules 25:745. https://doi.org/10.3390/molecules25030745
Del Sol R, Armstrong I, Wright C et al (2007) Characterization of changes to the cell surface during the life cycle of Streptomyces coelicolor: atomic force microscopy of living cells. J Bacteriol 189:2219–2225. https://doi.org/10.1128/JB.01470-06
Drzyzga O (2012) The strengths and weaknesses of Gordonia: a review of an emerging genus with increasing biotechnological potential. Crit Rev Microbiol 38:300–316. https://doi.org/10.3109/1040841X.2012.668134
Evstigneeva A, Raoult D, Karpachevskiy L et al (2009) Amoeba co-culture of soil specimens recovered 33 different bacteria, including four new species and Streptococcus pneumoniae. Microbiology 155:657–664. https://doi.org/10.1099/mic.0.022970-0
Ferrari BC, Winsley T, Gillings M et al (2008) Cultivating previously uncultured soil bacteria using a soil substrate membrane system. Nat Protoc 3:1261–1269. https://doi.org/10.1038/nprot.2008.102
Francisco OA, Glor HM, Khajehpour M (2020) Salt effects on hydrophobic solvation: is the observed salt specificity the result of excluded volume effects or water mediated ion-hydrophobe association? Chem Phys Chem 21:484–493. https://doi.org/10.1002/cphc.201901000
Gavrish E, Bollmann A, Epstein S et al (2008) A trap for in-situ cultivation of filamentous actinobacteria. J Microbiol Methods 72:257–262. https://doi.org/10.1016/j.mimet.2007.12.009
Goldstein JI, Newbury DE, Echlin P et al (1992) Coating and conductivity techniques for SEM and microanalysis. In: Scanning electron microscopy and X-ray microanalysis. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0491-3_13
Guimarães TC, Gomes TS, Fernandes CD et al (2020) Antitumor microbial products by actinomycetes isolated from different environments. In: Arora PK (ed) Microbial technology for health and environment, 1st edn. Springer, Singapore, pp 113–160
Hahn MW, Koll U, Schmidt J (2019) Isolation and cultivation of bacteria. In: Hurst, Christon J (ed) The structure and function of aquatic microbial communities, 1 st edn. Springer, Switzerland AG, pp 313–351
Hamedi J, Imanparast S, Mohammadipanah F (2015) Molecular, chemical and biological screening of soil actinomycete isolates in seeking bioactive peptide metabolites. Iran J Microbiol 7:23–30
Hamedi J, Kafshnouchi M, Ranjbaran M (2019) A study on actinobacterial diversity of Hampoeil cave and screening of their biological activities. Saudi J Biol Sci 26:1587–1595. https://doi.org/10.1016/j.sjbs.2018.10.010
Jin Y, Gan G, Yu X et al (2017) Isolation of viable but non-culturable bacteria from printing and dyeing wastewater bioreactor based on resuscitation promoting factor. Curr Microbiol 74:787–797. https://doi.org/10.1007/s00284-017-1240-z
Kaeberlein T, Lewis K, Epstein SS (2002) Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:1127–1129. https://doi.org/10.1126/science.1070633
Kato S, Yamagishi A, Daimon S et al (2018) Isolation of previously uncultured slow-growing bacteria by using a simple modification in the preparation of agar media. Appl Environ Microbiol 84:e00807-e818. https://doi.org/10.1128/AEM.00807-18
Kodani S, Sato K, Hemmi H et al (2014) Isolation and structural determination of a new hydrophobic peptide venepeptide from Streptomyces venezuelae. J Antibiot 67:839–842. https://doi.org/10.1038/ja.2014.81
Kumar V, Bisht GS, Institu SBSP (2010) An improved method for isolation of genomic DNA from filamentous actinomycetes. Int J Eng Technol Manage Appl Sci 41:1383–1389. https://doi.org/10.1590/S0103-84782011000800014
Kurahashi M, Fukunaga Y, Sakiyama Y et al (2009) Iamia majanohamensis gen. nov., sp. nov., an actinobacterium isolated from sea cucumber Holothuria edulis, and proposal of Iamiaceae fam. nov. Int J Syst Evol Microbiol 59:869–873. https://doi.org/10.1099/ijs.0.005611-0
Lewis WH, Ettema TJ (2019) Culturing the uncultured. Nat Biotechnol 37:278–1279. https://doi.org/10.1038/s41587-019-0300-2
Mohammadipanah F, Matasyoh J, Hamedi J et al (2012) Persipeptides A and B, two cyclic peptides from Streptomyces sp. UTMC 1154. Bioorg Med Chem 20:335–339. https://doi.org/10.1016/j.bmc.2011.10.076
Orr IG, Hadar Y, Sivan A (2004) Colonization, biofilm formation and biodegradation of polyethylene by a strain of Rhodococcus ruber. Appl Microbiol Biotechnol 65:97–104. https://doi.org/10.1007/s00253-004-1584-8
Overmann J, Abt B, Sikorski J (2017) Present and future of culturing bacteria. Annu Rev Microbiol 71:711–730. https://doi.org/10.1146/annurev-micro-090816-093449
Parris N, Sykes M, Dickey LC et al (2002) Recyclable zein-coated kraft paper and linerboard. Prog Paper Recycl 11:24–29
Petráčková D, Buriánková K, Tesařová E et al (2013) Surface hydrophobicity and roughness influences the morphology and biochemistry of streptomycetes during attached growth and differentiation. FEMS Microbiol Lett 342:147–156. https://doi.org/10.1111/1574-6968.12129
Polkade AV, Mantri SS, Patwekar UJ et al (2016) Quorum sensing: an under-explored phenomenon in the phylum Actinobacteria. Front Microbiol 7:131. https://doi.org/10.3389/fmicb.2016.00131
Pridham TG, Anderson P, Foley C et al (1957) A selection of media for maintenance and taxonomic study of streptomycetes. Antibiot Annu 1956:947–953
Pulschen AA, Bendia AG, Fricker AD et al (2017) Isolation of uncultured bacteria from antarctica using long incubation periods and low nutritional media. Front Microbiol 8:1346. https://doi.org/10.3389/fmicb.2017.01346
Ravi K, García-Hidalgo J, Brink DP et al (2019) Physiological characterization and sequence analysis of a syringate-consuming Actinobacterium. Biores Tchnol 285:121327. https://doi.org/10.1016/j.biortech.2019.121327
Raynal A, Karray F, Tuphile K et al (2006) Excisable cassettes: new tools for functional analysis of Streptomyces genomes. Appl Environ Microbiol 72:4839–4844. https://doi.org/10.1128/AEM.00167-06
Reynaud C, Tapin-Lingua S, Elegir G et al (2013) Hydrophobic properties conferred to Kraft pulp by a laccase-catalysed treatment with lauryl gallate. J Biotechnol 167:302–308. https://doi.org/10.1016/j.jbiotec.2013.07.014
Salimi F, Hamedi J, Motevaseli E et al (2018) Isolation and screening of rare Actinobacteria, a new insight for finding natural products with antivascular calcification activity. J Appl Microbiol 124:254–266. https://doi.org/10.1111/jam.13605
Schofield C (2015) Antibiotics: current innovations and future trends. Caister Academic Press, U.K.
Singh AP, Dawson BS (2010) Probing the wood coating interface at high resolution. In: editors. Delamination in wood, wood products and wood-based composites, Springer, pp 145–157
Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231
Subramani R, Sipkema D (2019) Marine rare actinomycetes: a promising source of structurally diverse and unique novel natural products. Mar Drugs 17:249. https://doi.org/10.3390/md17050249
Twede D (2005) The origins of paper based packaging. In: Conference on historical analysis and research in marketing proceedings, vol. 12, pp 288–300
Whitman WB, Goodfellow M, Kampfer P (2012) Bergey’s manual of systematic bacteriology: Volume 5, The Actinobacteria. Springer, New York
Wink J, Mohammadipanah F, Hamedi J (2017) Biology and biotechnology of actinobacteria. Springer, Berlin
Zeinali M, Vossoughi M, Ardestani SK et al (2007) Hydrocarbon degradation by thermophilic Nocardia otitidiscaviarum strain TSH1: physiological aspects. J Basic Microbiol 47:534–539. https://doi.org/10.1002/jobm.200700283
Zhang B, Wu X, Tai X et al (2019) Variation in actinobacterial community ccomposition and potential function in different soil ecosystems belonging to the arid Heihe River Basin of Northwest China. Front Microbiol 10:2209–2220. https://doi.org/10.3389/fmicb.2019.02209
Acknowledgements
The authors wish to thank Leila Parvizi and Fahimeh Mohammadnia (Tooka Biotechnology Development Co.) for their technical assistance, Ali Aziminejad for his assistance in container preparation, and Behzad Ghomi and Fardin Hassandoost (from Maragheh Caving Club, Maragheh Etehad Caving Group) for their sincere cooperation in sample collection.
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Almasi, F., Kafshnouchi, M., Mohammadipanah, F. et al. Fruit wrapping kraft coated paper promotes the isolation of actinobacteria using ex situ and in situ methods. Folia Microbiol 66, 1047–1054 (2021). https://doi.org/10.1007/s12223-021-00907-8
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DOI: https://doi.org/10.1007/s12223-021-00907-8