Abstract
Soil-borne pathogens cause severe diseases in many crops around the world. Due to the harmful nature of the chemical pesticides used against such pathogens, extensive research has focused on developing sustainable solutions such as biocontrol agents. Nevertheless, the complex interaction of such agents with their biotic and abiotic environment is challenging. Filamentous cyanobacteria, the pioneers and main primary producers in biological soil crusts (BSC), show considerable tolerance to extreme environmental conditions within the crust. Soil inoculation with cyanobacteria is a promising practice for sustainable agriculture in drylands where high tolerant organisms is required. Nevertheless, its plant protection potential has been less explored. Cyanobacteria such as Leptolyngbya ohadii, a dominant species in the BSC of the northwest Negev desert, Israel, are known to produce a large array of secondary metabolites. Application of L.ohadii spent media severely inhibits the growth of various prokaryotes and eukaryotes. Its resilience and the observed antimicrobial activity thus make L.ohadii a promising candidate for the development of a biocontrol agent. However, little is known about the effect of environmental conditions on its antimicrobial activity. Here we examined the antifungal activity of L.ohadii on a range of soil-borne fungal pathogens. We assessed the effect of the daily hydration/dehydration cycle of its natural habitat on the expression of gene clusters for secondary metabolites production using a novel custom-made environmental conditions simulation chamber. Our data advance the understanding of the complex interaction of L.ohadii with its biotic and abiotic environment for application as a dryland biocontrol agent.
Similar content being viewed by others
Data availability
Mapping of the antiSMASH predicted genes to the L.ohadii transcriptome is provided as a csv file as a supplementary information. Photos of fungal growth analaysis by ColonyArea plugin is provided as a tif files.
References
Alsharif, W., Saad, M. M., & Hirt, H. (2020). Desert Microbes for Boosting Sustainable Agriculture in Extreme Environments. Frontiers in Microbiology, 11(July). https://doi.org/10.3389/fmicb.2020.01666
Anwer, M. A., Singh, K., Prasad, B. D., Yadav, A. K., & Kumari, P. (2020). Abiotic Stress Tolerant Trichoderma asperellum Tvb1 from Hot Spring and its Antagonistic Potential Against Soil Borne Phytopathogens. International Archive of Applied Sciences and Technology, 11(September), 70–90. https://doi.org/10.15515/iaast.0976-4828.11.3.7090
Belnap, J., Weber, B., & Büdel, B. (2016). Biological Soil Crusts as an Organizing Principle in Drylands (pp. 3–13). https://doi.org/10.1007/978-3-319-30214-0_1
Ben-Gal, A., Tal, A., & Tel-Zur, N. (2006). The sustainability of arid agriculture: Trends and challenges. Annals of Arid Zone, 45(3–4), 227–257.
Blin, K., Shaw, S., Kloosterman, A. M., Charlop-Powers, Z., van Wezel, G. P., Medema, M. H., & Weber, T. (2021). antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Research, 49(May), 29–35. https://doi.org/10.1093/nar/gkab335
Daryaei, A., Jones, E. E., Ghazalibiglar, H., Glare, T. R., & Falloon, R. E. (2016). Effects of temperature, light and incubation period on production, germination and bioactivity of Trichoderma atroviride. Journal of Applied Microbiology, 120(4), 999–1009. https://doi.org/10.1111/jam.13076
Fushimi, K., Rockwell, N. C., Enomoto, G., Ni-Ni-Win S. S. M., Gan, F., Bryant, D. A., Ikeuchi, M., Lagarias, J. C., & Narikawa, R. (2016). Cyanobacteriochrome Photoreceptors Lacking the Canonical Cys Residue. Biochemistry, 55(50), 6981-6995. https://doi.org/10.1021/acs.biochem.6b00940
Guzmán, C., Bagga, M., Kaur, A., Westermarck, J., & Abankwa, D. (2014). ColonyArea: An ImageJ plugin to automatically quantify colony formation in clonogenic assays. PLoS ONE, 9(3), 14–17. https://doi.org/10.1371/journal.pone.0092444
Hagemann, M., Henneberg, M., Felde, V. J. M. N. L., Drahorad, S. L., Berkowicz, S. M., Felix-Henningsen, P., & Kaplan, A. (2015). Cyanobacterial Diversity in Biological Soil Crusts along a Precipitation Gradient, Northwest Negev Desert Israel. Microbial Ecology, 70(1), 219–230. https://doi.org/10.1007/s00248-014-0533-z
Huang, J., Yu, H., Guan, X., Wang, G., & Guo, R. (2016). Accelerated dryland expansion under climate change. Nature Climate Change, 6(2), 166–171. https://doi.org/10.1038/nclimate2837
Hübschmann, T., Yamamoto, H., Gieler, T., Murata, N., & Börner, T. (2005). Red and far-red light alter the transcript profile in the cyanobacterium Synechocystis sp. PCC 6803: Impact of cyanobacterial phytochromes. FEBS Letters, 579(7), 1613–1618. https://doi.org/10.1016/j.febslet.2005.01.075
Katan, J. (2017). Diseases caused by soilborne pathogens: Biology, management and challenges. Journal of Plant Pathology, 99(2), 305–315. https://doi.org/10.4454/jpp.v99i2.3862
Kedem, I., Treves, H., Noble, G., Hagemann, M., Murik, O., Raanan, H., Oren, N., Giordano, M., & Kaplan, A. (2020). Keep your friends close and your competitors closer: Novel interspecies interaction in desert biological sand crusts. Phycologia, 00(00), 1–8. https://doi.org/10.1080/00318884.2020.1843349
Lamparter, T. (2004). Evolution of cyanobacterial and plant phytochromes. FEBS Letters, 573(1–3), 1–5. https://doi.org/10.1016/j.febslet.2004.07.050
Lee, S.-M., & Ryu, C.-M. (2021). Algae as New Kids in the Beneficial Plant Microbiome. Frontiers in Plant Science, 12(February), 1–18. https://doi.org/10.3389/fpls.2021.599742
Mazzola, M., & Freilich, S. (2017). Prospects for biological soilborne disease control: Application of indigenous versus synthetic microbiomes. Phytopathology, 107(3), 256–263. https://doi.org/10.1094/PHYTO-09-16-0330-RVW
Nagano, S. (2016). From photon to signal in phytochromes: Similarities and differences between prokaryotic and plant phytochromes. Journal of Plant Research, 129(2), 123–135. https://doi.org/10.1007/s10265-016-0789-0
Oren, N., Raanan, H., Kedem, I., Turjeman, A., Bronstein, M., Kaplan, A., & Murik, O. (2019). Desert cyanobacteria prepare in advance for dehydration and rewetting: The role of light and temperature sensing. Molecular Ecology, 28(9), 2305–2320. https://doi.org/10.1111/mec.15074
Oren, N., Raanan, H., Murik, O., Keren, N., & Kaplan, A. (2017). Dawn illumination prepares desert dehydration. Current Biology, 27(19), R1056–R1057. https://doi.org/10.1016/j.cub.2017.08.027
Pittelkow, C. M., Linquist, B. A., Lundy, M. E., Liang, X., van Groenigen, K. J., Lee, J., van Gestel, N., Six, J., Venterea, R. T., & van Kessel, C. (2015). When does no-till yield more? A global meta-analysis. Field Crops Research, 183, 156–168. https://doi.org/10.1016/j.fcr.2015.07.020
Raanan, H., Oren, N., Treves, H., Berkowicz, S. M., Hagemann, M., Pade, N., Keren, N., & Kaplan, A. (2016). Simulated soil crust conditions in a chamber system provide new insights on cyanobacterial acclimation to desiccation. Environmental Microbiology, 18(2), 414–426. https://doi.org/10.1111/1462-2920.12998
Renuka, N., Guldhe, A., Prasanna, R., Singh, P., & Bux, F. (2018). Microalgae as multi-functional options in modern agriculture: Current trends, prospects and challenges. Biotechnology Advances, 36(4), 1255–1273. https://doi.org/10.1016/j.biotechadv.2018.04.004
Rodriguez-Caballero, E., Belnap, J., Büdel, B., Crutzen, P. J., Andreae, M. O., Pöschl, U., & Weber, B. (2018). Dryland photoautotrophic soil surface communities endangered by global change. Nature Geoscience, 11(3), 185–189. https://doi.org/10.1038/s41561-018-0072-1
Rutledge, P. J., & Challis, G. L. (2015). Discovery of microbial natural products by activation of silent biosynthetic gene clusters. Nature Reviews Microbiology, 13(8), 509–523. https://doi.org/10.1038/nrmicro3496
Skaalsveen, K., Ingram, J., & Clarke, L. E. (2019). The effect of no-till farming on the soil functions of water purification and retention in north-western Europe: A literature review. Soil and Tillage Research, 189(January), 98–109. https://doi.org/10.1016/j.still.2019.01.004
Van Goethem, M. W., Osborn, A. R., Bowen, B. P., Andeer, P. F., Swenson, T. L., Clum, A., Riley, R., He, G., Koriabine, M., Sandor, L., Yan, M., Daum, C. G., Yoshinaga, Y., Makhalanyane, T. P., Garcia-Pichel, F., Visel, A., Pennacchio, L. A., O’Malley, R. C., & Northen, T. R. (2021). Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics. Communications Biology, 4(1), 2–11. https://doi.org/10.1038/s42003-021-02809-4
Xu, H.-F., Raanan, H., Dai, G.-Z., Oren, N., Berkowicz, S., Murik, O., Kaplan, A., & Qiu, B.-S. (2021). Reading and surviving the harsh conditions in desert biological soil crust: the cyanobacterial viewpoint. FEMS Microbiology Reviews, June, 1–19. https://doi.org/10.1093/femsre/fuab036
Acknowledgements
We thank the Jewish Charitable Association (ICA Israel) for funding this research in the framework of the project “Towards a sustainable soilborne pathogen biocontrol agent: Exploring the potential of soil Cyanobacteria isolated from Biological Soil Crusts” (Grant number 132218523)
Funding
Partial financial support was received from the Jewish Charitable Association (ICA Israel) in the framework of the project “Towards a sustainable soilborne pathogen biocontrol agent: Exploring the potential of soil Cyanobacteria isolated from Biological Soil Crusts” (Grant number 132218523).
Author information
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
All authors reviewed the manuscript and agreed for publication.
Competing interests
The authors have no competing interests to declare that are relevant to the content of this article.
Financial interest
-The authors have no relevant financial or non-financial interests to disclose.
-All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.
-The authors have no financial or proprietary interests in any material discussed in this article.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Margolis, N., Eckstien, D., Oren, N. et al. Towards a dryland biocontrol agent: Exploring the potential of the soil cyanobacterium Leptolyngbya ohadii isolated from biological soil crusts. Phytoparasitica 51, 717–725 (2023). https://doi.org/10.1007/s12600-022-01031-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12600-022-01031-0