journal article·2019-05-26Open access

The Study on the Cultivable Microbiome of the Aquatic Fern Azolla Filiculoides L. as New Source of Beneficial Microorganisms

Artur Banach, Agnieszka Kuźniar, Radosław Mencfel, Agnieszka Wolińska

Applied Sciences· Volume 9· Issue 10

Abstract

The aim of the study was to determine the still not completely described microbiome associated with the aquatic fern Azolla filiculoides. During the experiment, 58 microbial isolates (43 epiphytes and 15 endophytes) with different morphologies were obtained. We successfully identified 85% of microorganisms and assigned them to 9 bacterial genera: Achromobacter, Bacillus, Microbacterium, Delftia, Agrobacterium, and Alcaligenes (epiphytes) as well as Bacillus, Staphylococcus, Micrococcus, and Acinetobacter (endophytes). We also studied an A. filiculoides cyanobiont originally classified as Anabaena azollae; however, the analysis of its morphological traits suggests that this should be renamed as Trichormus azollae. Finally, the potential of the representatives of the identified microbial genera to synthesize plant growth-promoting substances such as indole-3-acetic acid (IAA), cellulase and protease enzymes, siderophores and phosphorus (P) and their potential of utilization thereof were checked. Delftia sp. AzoEpi7 was the only one from all the identified genera exhibiting the ability to synthesize all the studied growth promoters; thus, it was recommended as the most beneficial bacteria in the studied microbiome. The other three potentially advantageous isolates (Micrococcus sp. AzoEndo14, Agrobacterium sp. AzoEpi25 and Bacillus sp. AzoEndo3) displayed 5 parameters: IAA (excluding Bacillus sp. AzoEndo3), cellulase, protease, siderophores (excluding Micrococcus sp. AzoEndo14), as well as mineralization and solubilization of P (excluding Agrobacterium sp. AzoEpi25).
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Research context

OpenAlex topics: Biological Control of Invasive Species · Constructed Wetlands for Wastewater Treatment · Coastal wetland ecosystem dynamics

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Biochemistry and Environmental Chemistry, The John Paul II Catholic University of Lublin, 20-708 Lublin, Poland

Department of Animal Physiology and Toxicology, The John Paul II Catholic University of Lublin, 20-708 Lublin, Poland

References (60)

Show source-provided references
1. The wheat microbiome under four management strategies, and potential for endophytes in disease control10.1094/PBIOMES-05-17-0023-R ↗
3. The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes10.1128/MMBR.00050-14 ↗
4. The plant microbiome explored: Implications for experimental botany10.1093/jxb/erv466 ↗
5. Characterization of the cultivable bacterial populations associated with field grown Brassica napus L.: An evaluation of sampling and isolation protocols10.1111/1462-2920.12701 ↗
6. Plant growth-promoting bacterial endophytes10.1016/j.micres.2015.11.008 ↗
7. Parvaiz, A. (2016). Microbially assisted phytoremediation of heavy metal–contaminated soils. Plant Metal Interaction. Emerging Remediation Techniques, Elsevier Inc.
8. Synthesis of siderophores by plant-associated metallotolerant bacteria under exposure to Cd2+10.1016/j.chemosphere.2016.04.130 ↗
9. Plant Growth-Promoting Bacteria: Mechanisms and Applications
10. Azolla as a Superorganism. Its Implication in Symbiotic Studies10.1007/978-90-481-9449-0_11 ↗
11. Phytoremediation as a promising technology for water and soil purification: Azolla caroliniana Willd. As a case study
12. Phytoremediation Potential of Aquatic Macrophyte, Azolla10.1007/s13280-011-0159-z ↗
13. DNA probes show genetic variation in cyanobacterial symbionts of the Azolla fern and a closer relationship to free-living Nostoc strains than to free-living Anabaena strains10.1128/aem.56.5.1263-1270.1990 ↗
14. Identification of a common cyanobacterial symbiont associated with Azolla spp. through molecular and morphological characterization of free-living and symbiotic cyanobacteria10.1128/aem.57.8.2141-2146.1991 ↗
15. The cyanobiont in an Azolla fern is neither Anabaena nor Nostoc10.1016/S0378-1097(03)00784-5 ↗
16. Classification and phylogeny of the cyanobiont Anabaena azollae Strasburger: An answered question?10.1099/ijs.0.059238-0 ↗
17. Infrastrutture di Anabaena azollae vivente nelle foglioline di Azolla caroliniana (in Italian)
18. Occurrence and Ultrastructural Characterization of Bacteria in Association with and Isolated from Azolla caroliniana10.1128/aem.57.12.3629-3636.1991 ↗
19. Are bacteria the third partner of the Azolla-Anabaena symbiosis?10.1007/BF02187448 ↗
20. The Presence of Lectins in Bacteria Associated with the Azolla-Anabaena Symbiosis
21. Zagajewski, P. (2012). Influence of environmental factors on growth and toxin production by cyanobacterial species (in Polish). [Ph.D. Thesis, Adam Mickiewicz University Poznań. Faculty of Biology, Department of Water Protection].
22. Phylogenetic and taxonomic position of the genus Wollea with the description of Wollea salina sp. nov. (Cyanobacteria, Nostocales)10.5507/fot.2015.026 ↗
23. Antifungal compounds from cyanobacteria10.3390/md13042124 ↗
24. Phylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomenon
25. Morphological and molecular characterization of planktonic cyanobacteria from Belgium and Luxembourg10.1111/j.1529-8817.2006.00284.x ↗
26. Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify10.1111/nph.14843 ↗
27. Modern approach to the classification system of cyanophytes
28. Canter-Lund, H., and Lund, J.W.G. (1995). Freshwater Algae: Their Microscopic World Explored, Biopress Ltd.
29. Guiry, M.D., and Guiry, G.M. (2019, April 15). AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available online: http://www.algaebase.org/search/species/detail/?species_id=65456.
30. Indole-3-acetic acid (IAA) production by Arthrobacter species isolated from Azolla10.1099/00221287-138-2-377 ↗
31. Isolation and characterization of rhizobacteria and their effects on root extracts of Valeriana officinalis
32. Assessment of Culturable Tea Rhizobacteria Isolated from Tea Estates of Assam, India for Growth Promotion in Commercial Tea Cultivars10.3389/fmicb.2015.01252 ↗
33. Revealing the biotechnological potential of Delftia sp. JD2 by a genomic approach10.3934/bioeng.2016.2.156 ↗
34. Endophytic Bacterial Communities in Ginseng and their Antifungal Activity Against Pathogens10.1007/s00248-007-9208-3 ↗
35. Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in a volcanic soil10.1007/s00374-008-0288-0 ↗
36. Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities10.1016/j.apsoil.2005.12.002 ↗
37. Inoculation of soil with cadmium-resistant bacterium Delftia sp. B9 reduces cadmium accumulation in rice (Oryza sativa L.) grains10.1016/j.ecoenv.2018.07.081 ↗
38. Potential biodegradation of phenanthrene by isolated halotolerant bacterial strains from petroleum oil polluted soil in Yellow River Delta10.1016/j.scitotenv.2019.02.080 ↗
39. Castro-Sowinski, S. (2016). The sustainable use of Delftia in agriculture, bioremediation, and bioproducts synthesis. Microbial Models: From Environmental to Industrial Sustainability, Springer. [1st ed.].
40. Genome sequencing reveals mechanisms for heavy metal resistance and polycyclic aromatic hydrocarbon degradation in Delftia lacustris strain LZ-C10.1007/s10646-015-1583-9 ↗
41. Draft genome sequence of Delftia tsuruhatensis MTQ3, a strain of plant growth-promoting rhizobacterium with antimicrobial activity10.1128/genomeA.00822-15 ↗
42. Gold biomineralization by a metallophore from a gold-associated microbe10.1038/nchembio.1179 ↗
43. Extracellular Biomineralization of Gold by Delftia tsuruhatensis GX-3 Isolated from a Heavy Metal Contaminated Paddy Soil10.1021/acsearthspacechem.8b00127 ↗
44. Isolation and Characterization of Electrochemically Active Subsurface Delftia and Azonexus Species10.3389/fmicb.2016.00756 ↗
45. Nanopods: A New Bacterial Structure and Mechanism for Deployment of Outer Membrane Vesicles10.1371/journal.pone.0020725 ↗
46. Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: A review10.1007/s13205-014-0206-0 ↗
47. Watanabe, I., Roger, P.A., Ladha, J.K., and Van Hove, C. (1992). Biofertilizer germplasm collections at IRRI, International Rice Research Institute.
48. Cyanoprokaryota: 3rd Part: Heterocystous Genera
49. Hindák, F. (2001). Fotografický atlas mikroskopických sinic (in Slovak), VEDA.
50. Enrichment culture and identification of endophytic methanotrophs isolated from peatland plants10.1007/s12223-017-0508-9 ↗
51. Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana10.1111/j.1438-8677.2012.00711.x ↗
52. A Rapid and Easy Method for the Detection of Microbial Cellulases on Agar Plates Using Gram’s Iodine10.1007/s00284-008-9276-8 ↗
53. Use of chrome azurol S reagents to evaluate siderophore production by rhizsphere bacteria10.1007/BF00369386 ↗
54. Sambrook, J., and Russell, R.W. (2001). Molecular cloning: A laboratory manual, Cold Spring Harbor Laboratory Press. [3rd ed.].
55. Colorimetric estimation of indoleacetic acid10.1104/pp.26.1.192 ↗
56. Discovery of commonly existing anode biofilm microbes in two different wastewater treatment MFCs using FLX Titanium pyrosequencing10.1007/s00253-010-2680-6 ↗
57. Cyanobacterial Diversity in Natural and Artificial Microbial Mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): A Morphological and Molecular Approach
58. Quantitative Real-Time PCR Detection of Toxic Nodularia Cyanobacteria in the Baltic Sea10.1128/AEM.02746-06 ↗
59. PCR Primers To Amplify 16S rRNA Genes from Cyanobacteria10.1128/aem.63.8.3327-3332.1997 ↗
60. NifH and NifD phylogenies: An evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria10.1099/mic.0.26585-0 ↗