The Root Microbiome of Salicornia ramosissima as a Seedbank for Plant-Growth Promoting Halotolerant Bacteria
Source abstract
Abstract
Root−associated microbial communities play important roles in the process of adaptation of plant hosts to environment stressors, and in this perspective, the microbiome of halophytes represents a valuable model for understanding the contribution of microorganisms to plant tolerance to salt. Although considered as the most promising halophyte candidate to crop cultivation, Salicornia ramosissima is one of the least-studied species in terms of microbiome composition and the effect of sediment properties on the diversity of plant-growth promoting bacteria associated with the roots. In this work, we aimed at isolating and characterizing halotolerant bacteria associated with the rhizosphere and root tissues of S. ramosissima, envisaging their application in saline agriculture. Endophytic and rhizosphere bacteria were isolated from wild and crop cultivated plants, growing in different estuarine conditions. Isolates were identified based on 16S rRNA sequences and screened for plant-growth promotion traits. The subsets of isolates from different sampling sites were very different in terms of composition but consistent in terms of the plant-growth promoting traits represented. Bacillus was the most represented genus and expressed the wider range of extracellular enzymatic activities. Halotolerant strains of Salinicola, Pseudomonas, Oceanobacillus, Halomonas, Providencia, Bacillus, Psychrobacter and Brevibacterium also exhibited several plant-growth promotion traits (e.g., 3-indole acetic acid (IAA), 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, siderophores, phosphate solubilization). Considering the taxonomic diversity and the plant-growth promotion potential of the isolates, the collection represents a valuable resource that can be used to optimize the crop cultivation of Salicornia under different environmental conditions and for the attenuation of salt stress in non-halophytes, considering the global threat of arable soil salinization.
Source: crossref · Quality: baseline
Research context
OpenAlex topics: Plant-Microbe Interactions and Immunity · Microbial Community Ecology and Physiology · Nematode management and characterization studies
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Department of Biology and CESAM, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
Department of Geosciences and Geobiotec, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
Funding
Fundação para a Ciência e a Tecnologia · Centro de Estudos Ambientais e Marinhos, Universidade de Aveiro
References (98)
Show source-provided references
1. Yuan, Z., Druzhinina, I.S., Labbé, J., Redman, R., Qin, Y., Rodriguez, R., Zhang, C., Tuskan, G.A., and Lin, F. (2016). Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. Sci. Rep., 6.10.1038/srep32467 ↗
2. Salinity tolerance in halophytes10.1111/j.1469-8137.2008.02531.x ↗
3. Editorial: Salinity tolerance in plants: Mechanisms and regulation of ion transport10.3389/fpls.2017.01795 ↗
4. Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera10.1007/s00253-009-2116-3 ↗
5. The Sphagnum microbiome supports bog ecosystem functioning under extreme conditions10.1111/mec.12885 ↗
6. The role of plant-microbiome interactions in weed establishment and control10.1093/femsec/fiw138 ↗
7. Deciphering composition and function of the root microbiome of a legume plant10.1186/s40168-016-0220-z ↗
8. Salt-Tolerant Plant Growth Promoting Rhizobacteria for Enhancing Crop Productivity of Saline Soils10.3389/fmicb.2019.02791 ↗
9. Plant-rhizobacteria interactions alleviate abiotic stress conditions10.1111/j.1365-3040.2009.02028.x ↗
10. The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential10.1007/s11104-011-0877-9 ↗
11. Properties of the halophyte microbiome and their implications for plant salt tolerance10.1071/FP12355 ↗
12. Salicornia L.10.1016/B978-0-444-89215-7.50096-8 ↗
13. Salicornia ramosissima population dynamics and tolerance of salinity10.1007/s11284-006-0008-x ↗
14. Jefferies, R.L., and Gottlieb, L.D. (1982). Genetic differentiation of the microspecies Salicornia europaea L. (sensu stricto) and S. ramosissima. J. Woods. New Phytol.10.1111/j.1469-8137.1982.tb03368.x ↗
15. Milić, D., Luković, J., Dan, M., Zorić, L., Obreht, D., Veselić, S., Anačkov, G., and Petanidou, T. (2011). Identification of salicornia population: Anatomical characterization and RAPD fingerprinting. Arch. Biol. Sci.10.2298/ABS1104087M ↗
16. Ingrouille, M., and Pearson, J. (1987). The pattern of morphological variation in the Salicornia europaea L. aggregate (Chenopodiaceae). Watsonia.
17. Bae, J.Y., Park, L.Y., and Lee, S.H. (2008). Effect of Salicornia herbacea L. powder on the quality characteristics of bread. J. Korean Soc. Food Sci. Nutr.10.3746/jkfn.2008.37.9.1196 ↗
18. Vacuum drying characteristics of Salicornia herbacea L.
19. Oil and Fatty Acids Composition in Glasswort (Salicornia Fruticosa) Seeds10.9790/5736-0450609 ↗
20. Lipophilic profile of the edible halophyte Salicornia ramosissima10.1016/j.foodchem.2014.05.117 ↗
21. Illumina-based analysis of bacterial diversity related to halophytes Salicornia europaea and Sueada aralocaspica10.1007/s12275-015-5080-x ↗
22. Bacterial and fungal endophytic microbiomes of Salicornia europaea10.1128/AEM.00305-19 ↗
23. Bacterial microbiome of root-associated endophytes of Salicornia europaea in correspondence to different levels of salinity10.1007/s11356-018-2530-0 ↗
24. Isolation of Endophytic Plant Growth-Promoting Bacteria Associated with the Halophyte Salicornia europaea and Evaluation of their Promoting Activity Under Salt Stress10.1007/s00284-016-1096-7 ↗
25. Improved growth and salinity tolerance of the halophyte Salicornia sp. by co–inoculation with endophytic and rhizosphere bacteria10.1016/j.apsoil.2019.02.022 ↗
26. Improved germination efficiency of Salicornia ramosissima seeds inoculated with Bacillus aryabhattai SP1016-2010.1111/aab.12495 ↗
27. Mesa-Marín, J., Pérez-Romero, J.A., Mateos-Naranjo, E., Bernabeu-Meana, M., Pajuelo, E., Rodríguez-Llorente, I.D., and Redondo-Gómez, S. (2019). Effect of plant growth-promoting rhizobacteria on salicornia ramosissima seed germination under salinity, CO2 and temperature stress. Agronomy, 9.10.3390/agronomy9100655 ↗
28. Plant growth-promoting activity and quorum quenching-mediated biocontrol of bacterial phytopathogens by Pseudomonas segetis strain P6
29. Effect of halotolerant endophytic bacteria isolated from Salicornia europaea L. on the growth of fodder beet (Beta vulgaris L.) under salt stress10.1080/03650340.2017.1286329 ↗
30. Salicornia europaea L. as an underutilized saline-tolerant plant inhabited by endophytic diazotrophs10.1016/j.jare.2019.05.002 ↗
31. Estimation of Soil Organic Matter by Weight Loss-On-Ignition
32. Zaman, M., Shahid, S.A., and Heng, L. (2018). Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques, Springer.10.1007/978-3-319-96190-3 ↗
33. Sonmez, S., Buyuktas, D., Okturen, F., and Citak, S. (2008). Assessment of different soil to water ratios (1:1, 1:2.5, 1:5) in soil salinity studies. Geoderma.10.1016/j.geoderma.2007.12.005 ↗
34. A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system10.1007/s13213-012-0491-y ↗
35. Life at High Salt Concentrations10.1007/0-387-30742-7_9 ↗
36. Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L.—Community structure and metabolic potential10.1016/j.micres.2016.05.012 ↗
37. 16S ribosomal DNA amplification for phylogenetic study10.1128/jb.173.2.697-703.1991 ↗
38. Cole, J.R., Wang, Q., Fish, J.A., Chai, B., McGarrell, D.M., Sun, Y., Brown, C.T., Porras-Alfaro, A., Kuske, C.R., and Tiedje, J.M. (2014). Ribosomal Database Project: Data and tools for high throughput rRNA analysis. Nucleic Acids Res.10.1093/nar/gkt1244 ↗
39. Agarwala, R., Barrett, T., Beck, J., Benson, D.A., Bollin, C., Bolton, E., Bourexis, D., Brister, J.R., Bryant, S.H., and Canese, K. (2017). Database Resources of the National Center for Biotechnology Information. Nucleic Acids Res.
40. Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., and Chun, J. (2017). Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol.10.1099/ijsem.0.001755 ↗
41. Brígido, C., Singh, S., Menéndez, E., Tavares, M.J., Glick, B.R., Do Rosário Félix, M., Oliveira, S., and Carvalho, M. (2019). Diversity and functionality of culturable endophytic bacterial communities in chickpea plants. Plants, 8.10.3390/plants8020042 ↗
42. Specific and sensitive plate assay for bacterial lipases10.1128/aem.53.1.211-213.1987 ↗
43. Biological control of Pythium ultimum by Stenotrophomonas maltophilia W81 is mediated by an extracellular proteolytic activity10.1099/00221287-143-12-3921 ↗
44. Colorimetric Estimation of Inodoleacetic Acid10.1104/pp.26.1.192 ↗
45. Effect of Indole-3-Acetic Acid (IAA) Produced by Pseudomonas aeruginosa in Suppression of Charcoal Rot Disease of Chickpea10.1007/s00284-009-9577-6 ↗
46. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria10.1034/j.1399-3054.2003.00086.x ↗
47. Metabolism of 1-aminocyclopropane-1-carboxylic acid
48. Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway10.1021/acschembio.5b00624 ↗
49. O-CAS, a fast and universal method for siderophore detection10.1016/j.mimet.2007.03.023 ↗
50. Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon10.1007/s003740050024 ↗
51. Isolation and characterization of phosphate solubilizing bacterium Pseudomonas aeruginosa KUPSB12 with antibacterial potential from river Ganga, India10.1016/j.aasci.2016.10.001 ↗
52. Plant Growth Promotion and Amelioration of Salinity Stress in Crop Plants by a Salt-Tolerant Bacterium
53. The correlation of carbon source and ammonium accumulation in culture broth by nitrogen-fixing bacterial isolates The correlation of carbon source and ammonium accumulation in culture broth by nitrogen-fixing bacterial isolates10.31254/jsir.2017.6205 ↗
54. A modified microtiter-plate test for quantification of staphylococcal biofilm formation10.1016/S0167-7012(00)00122-6 ↗
55. Characterization of adhesive exopolysaccharide (EPS) produced by Pseudomonas aeruginosa under starvation conditions10.1007/s00284-009-9365-3 ↗
56. R Core Team (2021, February 23). R: A Language and Environment for Statistical Computing. Available online: https://www.R-project.org.
57. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H., and Wagner, H. (2021, February 23). Vegan: Community Ecology Package. R Package Version 2.0-9. Available online: https://CRAN.R-project.org/package=vegan.
58. USDA (2017). Soil Survey Manual Agriculture. Handbook 18.
59. Rhoades, J., Kandiah, A., and Mashali, A. (1992). The Use of Saline Waters for Crop Production, Food and Agriculture Organization of the United Nations.
60. Etesami, H., and Beattie, G.A. (2018). Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front. Microbiol., 9.10.3389/fmicb.2018.00148 ↗
61. Szoboszlay, M., Näther, A., Liu, B., Carrillo, A., Castellanos, T., Smalla, K., Jia, Z., and Tebbe, C.C. (2019). Contrasting microbial community responses to salinization and straw amendment in a semiarid bare soil and its wheat rhizosphere. Sci. Rep.10.1038/s41598-019-46070-6 ↗
62. From cultured to uncultured genome sequences: Metagenomics and modeling microbial ecosystems10.1007/s00018-015-2004-1 ↗
63. Bacterial diversity associated with the rhizosphere and endosphere of two halophytes: Glaux maritima and Salicornia europaea10.3389/fmicb.2018.02878 ↗
64. Diversity of Endophytic Actinomycetes from Karangkadu Mangrove Ecosystem and Its Antibacterial Potential Against Bacterial Pathogens
65. Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition10.1016/j.soilbio.2004.08.005 ↗
66. Microbial Profiles of Rhizosphere and Bulk Soil Microbial Communities of Biofuel Crops Switchgrass (Panicum virgatum L.) and Jatropha (Jatropha curcas L.)10.1155/2012/906864 ↗
67. Differences in soil properties and bacterial communities between the rhizosphere and bulk soil and among different production areas of the medicinal plant Fritillaria thunbergii10.3390/ijms12063770 ↗
68. Mahmoudi, N., Beaupré, S.R., Steen, A.D., and Pearson, A. (2017). Sequential bioavailability of sedimentary organic matter to heterotrophic bacteria. Environ. Microbiol.10.1111/1462-2920.13745 ↗
69. Culturable endophytic bacteria from the salt marsh plant Halimione portulacoides: Phylogenetic diversity, functional characterization, and influence of metal(loid) contamination10.1007/s11356-016-6208-1 ↗
70. Biotechnological applications of bacterial cellulases10.3934/bioeng.2015.3.163 ↗
71. Mechanisms of action of plant growth promoting bacteria
72. Plant Growth-Promoting Bacteria: Mechanisms and Applications10.6064/2012/963401 ↗
73. Antagonistic and plant growth promoting activities of endophytic and soil actinomycetes10.1080/03235408.2013.777169 ↗
74. Etesami, H., and Alikhani, H.A. (2018). Bacillus species as the most promising bacterial biocontrol agents in rhizosphere and endorhiza of plants grown in rotation with each other. Eur. J. Plant Pathol.10.1007/s10658-017-1276-8 ↗
75. Metabolic potential and community structure of endophytic and rhizosphere bacteria associated with the roots of the halophyte Aster tripolium L.10.1016/j.micres.2015.09.007 ↗
76. Influence of varying degree of salinity-sodicity stress on enzyme activities and bacterial populations of coastal soils of yellow sea, South Korea10.4014/jmb.1012.12015 ↗
77. Microbial extracellular polymeric substances: Ecological function and impact on soil aggregation10.3389/fmicb.2018.01636 ↗
78. Upadhyay, S.K., Singh, J.S., and Singh, D.P. (2011). Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere.10.1016/S1002-0160(11)60120-3 ↗
79. Responses of microorganisms to osmotic stress10.1146/annurev-micro-020518-115504 ↗
80. Role of PGPR in Biofilm Formations and Its Importance in Plant Health10.1002/9781119246329.ch2 ↗
81. Short Term Influence of Salinity on Uptake of Phosphorus by Ipomoea aquatica
82. Microbially Mediated Plant Salt Tolerance and Microbiome-based Solutions for Saline Agriculture10.1016/j.biotechadv.2016.08.005 ↗
83. Phosphate solubilizing bacteria and their role in plant growth promotion10.1016/S0734-9750(99)00014-2 ↗
84. Exopolysaccharide: A novel important factor in the microbial dissolution of tricalcium phosphate10.1007/s11274-007-9575-4 ↗
85. Screening for rock phosphate solubilizing Actinomycetes from Moroccan phosphate mines10.1016/j.apsoil.2007.08.007 ↗
86. The Effect of Phosphorus in Nitrogen Fixation in Legumes
87. Interactive influence of phosphorus and iron on nitrogen fixation by soybean10.1016/j.envexpbot.2008.12.001 ↗
88. Mapelli, F., Marasco, R., Rolli, E., Barbato, M., Cherif, H., Guesmi, A., Ouzari, I., Daffonchio, D., and Borin, S. (2013). Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed Res. Int., 2013.10.1155/2013/248078 ↗
89. Cultivable Nitrogen Fixing Bacteria from Extremely Alkaline-Saline Soils10.4236/aim.2016.66041 ↗
90. Studies on salinization in Haryana soils on free-living nitrogen-fixing bacterial populations and their activity10.1002/jobm.201200158 ↗
91. Nitrogen Fixation in a Salt Marsh10.2307/2258998 ↗
92. Elmerich, C., and Newton, W.E. (2007). Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations. Assoc. Endophytic Nitrogen-Fixing Bact. Cyanobacterial Assoc.10.1007/1-4020-3546-2 ↗
93. Environmental and physiological controls on diel patterns of N2 fixation in epiphytic cyanobacterial communities10.1007/s002489900058 ↗
94. Indole-3-acetic acid (IAA) production trait, a useful screening to select endophytic and rhizosphere competent bacteria for rice growth promoting agents10.1016/j.mex.2015.02.008 ↗
95. Plant growth promoting rhizobacteria isolated from halophytes and drought-tolerant plants: Genomic characterisation and exploration of phyto-beneficial traits10.1038/s41598-020-71652-0 ↗
96. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria10.1006/jtbi.1997.0532 ↗
97. Oliveira, A.L.M., Canuto, E.L., Silva, E.E., Reis, V.M., and Baldani, J.I. (2004). Survival of endophytic diazotrophic bacteria in soil under different moisture levels. Braz. J. Microbiol.10.1590/S1517-83822004000300005 ↗
98. Han, L.L., Wang, Q., Shen, J.P., Di, H.J., Wang, J.T., Wei, W.X., Fang, Y.T., Zhang, L.M., and He, J.Z. (2019). Multiple factors drive the abundance and diversity of the diazotrophic community in typical farmland soils of China. FEMS Microbiol. Ecol.10.1093/femsec/fiz113 ↗