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- Endophytic Actinobacteria for Sustainable Agricultural ApplicationsPublication . Carvalho, M. F.; Ma, Y.; Oliveira, Rui S.; Freitas, H.Endophytic actinobacteria have the capacity to establish intimate associations with plants and colonize their inner tissues without causing apparent disease symptoms. They can protect plants by producing bioactive compounds that act as plant growth promoters or biological control agents and, in return, obtain nutrition and protection from the host plant. The application of endophytic actinobacteria in agriculture has attracted increasing attention. We address isolation and identification methods and the occurrence and diversity of endophytic actinobacteria in agricultural crops. Attention is given to the roles of endophytic actinobacteria in plant growth and development and health promotion for sustainable agriculture is discussed.
- Influence of mixtures of acenaphthylene and benzo[a] anthracene on their degradation by Pleurotus ostreatus in sandy soilPublication . Rocha, Inês; Pinto, Edgar; Ferreira, Isabel M. P. L. V. O.; Vieira Da Silva, Manuela; Oliveira, Rui S.Purpose Polycyclic aromatic hydrocarbons (PAHs) are a class of organic compounds commonly found as soil contaminants. Fungal degradation is considered as an environmentally friendly and cost-effective approach to remove PAHs from soil. Acenaphthylene (Ace) and Benzo[a]anthracene (BaA) are two PAHs that can coexist in soils; however, the influence of the presence of each other on their biodegradation has not been studied. The biodegradation of Ace and BaA, alone and in mixtures, by the white rot fungus Pleurotus ostreatus was studied in a sandy soil. Materials and methods Experimental microcosms containing soil spiked with different concentrations of Ace and BaAwere inoculated with P. ostreatus. Initial (t 0) and final (after 15 days of incubation) soil concentrations of Ace and BaA were determined after extraction of the PAHs. Results and discussion P. ostreatus was able to degrade 57.7% of the Ace in soil spiked at 30 mg kg−1 dry soil and 65.8% of Ace in soil spiked at 60 mg kg−1 dry soil. The degradation efficiency of BaA by P. ostreatus was 86.7 and 77.4% in soil spiked with Ace at 30 and 60 mg kg−1 dry soil, respectively. After 15 days of incubation, there were no significant differences in Ace concentration between soil spiked with Ace and soil spiked with Ace + BaA, irrespective of the initial soil concentration of both PAHs. There were also no differences in BaA concentration between soil spiked with BaA and soil spiked with BaA + Ace. Conclusions The results indicate that the fungal degradation of Ace and BaA was not influenced by the presence of each other’s PAH in sandy soil. Bioremediation of soils contaminated with Ace and BaA using P. ostreatus is a promising approach to eliminate these PAHs from the environment.
- Using microbial seed coating for improving cowpea productivity under a low‐input agricultural systemPublication . Rocha, Inês; Souza‐Alonso, Pablo; Pereira, Graça; Ma, Ying; Vosátka, Miroslav; Freitas, Helena; Oliveira, Rui S.BACKGROUND Plant‐growth‐promoting rhizobacteria (PGPR) and arbuscular mycorrhizal (AM) fungi have the ability to enhance the growth, fitness, and quality of various agricultural crops, including cowpea. However, field trials confirming the benefits of microbes in large‐scale applications using economically viable and efficient inoculation methods are still scarce. Microbial seed coating has a great potential for large‐scale agriculture through the application of reduced amounts of PGPR and AM fungi inocula. Thus, in this study, the impact of seed coating with PGPR, Pseudomonas libanensis TR1 and AM fungus, Rhizophagus irregularis (single or multiple isolates) on grain yield and nutrient content of cowpea under low‐input field conditions was evaluated. RESULTS Seed coating with P. libanensis + multiple isolates of R. irregularis (coatPMR) resulted in significant increases in shoot dry weight (76%), and in the number of pods and seeds per plant (52% and 56%, respectively) and grain yield (56%), when compared with non‐inoculated control plants. However, seed coating with P. libanensis + R. irregularis single‐isolate (coatPR) did not influence cowpea grain yield. Grain lipid content was significantly higher (25%) in coatPMR plants in comparison with control. Higher soil organic matter and lower pH were observed in the coatPMR treatment. CONCLUSIONS Our findings indicate that cowpea field productivity can be improved by seed coating with PGPR and multiple AM fungal isolates under low‐input agricultural systems. © 2019 Society of Chemical Industry
- Seed coating with inocula of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria for nutritional enhancement of maize under different fertilisation regimesPublication . Rocha, Inês; Ma, Ying; Carvalho, Maria F.; Magalhães, Catarina; Janoušková, Martina; Vosátka, Miroslav; Freitas, Helena; Oliveira, Rui S.Arbuscular mycorrhizal (AM) fungi and plant growth-promoting rhizobacteria, responsible for enhancing plant nutrition, vigour and growth, may be used to reduce dosages of chemical fertilisers. Technologies that allow an economically viable and efficient application of these beneficial microbes in large scale agriculture must be studied. Seed coating is a potential delivery system for efficiently introducing minor amounts of bioinoculants. Despite the dramatic reduction on inoculum dose per plant, inoculation of AM fungi via seed coating was as effective as conventional soil inoculation. Fertilisation and inoculation had a significant impact on maize shoots nutrient concentrations. Different fertilisation regimes did not influence mycorrhizal colonisation. Plants without fertilisation and singly inoculated with R. irregularis showed shoot nutrient concentration increments of 110, 93, 88 and 175% for nitrogen, phosphorus, potassium and zinc, respectively, comparing with non-inoculated controls. Plants singly inoculated with P. fluorescens via seed coating under full fertilisation, presented enhancements of 100, 75 and 141% for magnesium, zinc and manganese, respectively, comparing with non-inoculated controls. Seed coating is a promising tool for delivering microbial inoculants into the soil, while promoting sustainable production of maize. This technology is particularly pertinent in low input agriculture, with potential environmental profits and food quality improvements.
- The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soilPublication . Ma, Ying; Oliveira, Rui S.; Nai, Fengjiao; Rajkumar, Mani; Luo, Yongming; Rocha, Inês; Freitas, HelenaEndophyte-assisted phytoremediation has recently been suggested as a successful approach for ecological restoration of metal contaminated soils, however little information is available on the influence of endophytic bacteria on the phytoextraction capacity of metal hyperaccumulating plants in multi-metal polluted soils. The aims of our study were to isolate and characterize metal-resistant and 1-aminocyclopropane-1-carboxylate (ACC) utilizing endophytic bacteria from tissues of the newly discovered Zn/Cd hyperaccumulator Sedum plumbizincicola and to examine if these endophytic bacterial strains could improve the efficiency of phytoextraction of multi-metal contaminated soils. Among a collection of 42 metal resistant bacterial strains isolated from the tissues of S. plumbizincicola grown on Pb/Zn mine tailings, five plant growth promoting endophytic bacterial strains (PGPE) were selected due to their ability to promote plant growth and to utilize ACC as the sole nitrogen source. The five isolates were identified as Bacillus pumilus E2S2, Bacillus sp. E1S2, Bacillus sp. E4S1, Achromobacter sp. E4L5 and Stenotrophomonas sp. E1L and subsequent testing revealed that they all exhibited traits associated with plant growth promotion, such as production of indole-3-acetic acid and siderophores and solubilization of phosphorus. These five strains showed high resistance to heavy metals (Cd, Zn and Pb) and various antibiotics. Further, inoculation of these ACC utilizing strains significantly increased the concentrations of water extractable Cd and Zn in soil. Moreover, a pot experiment was conducted to elucidate the effects of inoculating metal-resistant ACC utilizing strains on the growth of S. plumbizincicola and its uptake of Cd, Zn and Pb in multi-metal contaminated soils. Out of the five strains, B. pumilus E2S2 significantly increased root (146%) and shoot (17%) length, fresh (37%) and dry biomass (32%) of S. plumbizincicola as well as plant Cd uptake (43%), whereas Bacillus sp. E1S2 significantly enhanced the accumulation of Zn (18%) in plants compared with non-inoculated controls. The inoculated strains also showed high levels of colonization in rhizosphere and plant tissues. Results demonstrate the potential to improve phytoextraction of soils contaminated with multiple heavy metals by inoculating metal hyperaccumulating plants with their own selected functional endophytic bacterial strains.
- Bioaugmentation with Endophytic Bacterium E6S Homologous to Achromobacter piechaudii Enhances Metal Rhizoaccumulation in Host Sedum plumbizincicolaPublication . Ma, Ying; Zhang, Chang; Oliveira, Rui S.; Freitas, Helena; Luo, YongmingApplication of hyperaccumulator-endophyte symbiotic systems is a potential approach to improve phytoremediation efficiency, since some beneficial endophytic bacteria are able to detoxify heavy metals, alter metal solubility in soil, and facilitate plant growth. The objective of this study was to isolate multi-metal resistant and plant beneficial endophytic bacteria and to evaluate their role in enhancing plant growth and metal accumulation/translocation. The metal resistant endophytic bacterial strain E6S was isolated from stems of the Zn/Cd hyperaccumulator plant Sedum plumbizincicola growing in metalliferous mine soils using Dworkin and Foster salts minimal agar medium with 1-aminocyclopropane-1-carboxylate (ACC) as the sole nitrogen source, and identified as homologous to Achromobacter piechaudii based on morphological and biochemical characteristics, partial 16S rDNA sequence and phylogenetic analysis. Strain E6S showed high level of resistance to various metals (Cd, Zn, and Pb). Besides utilizing ACC, strain E6S exhibited plant beneficial traits, such as solubilization of phosphate and production of indole-3-acetic acid. Inoculation with E6S significantly increased the bioavailability of Cd, Zn, and Pb in soil. In addition, bacterial cells bound considerable amounts of metal ions in the following order: Zn > Cd >Pb. Inoculation of E6S significantly stimulated plant biomass, uptake and bioaccumulation of Cd, Zn, and Pb. However, E6S greatly reduced the root to shoot translocation of Cd and Zn, indicating that bacterial inoculation assisted the host plant to uptake and store heavy metals in its root system. Inoculation with the endophytic bacterium E6S homologous to A. piechaudii can improve phytostabilization of metalliferous soils due to its effective ability to enhance in situ metal rhizoaccumulation in plants.
- Potential of plant beneficial bacteria and arbuscular mycorrhizal fungi in phytoremediation of metal-contaminated saline soilsPublication . Ma, Ying; Rajkumar, Mani; Oliveira, Rui S.; Zhang, Chang; Freitas, HelenaPhytoremediation has been considered as a promising technique to decontaminate polluted soils. However, climatic stress particularly salinity, is a potential threat to soil properties and plant growth, thus restricting the employment of this technology. The aim of this study was to access the impact of microbial inoculation on phytoremediation of nickel (Ni) contaminated saline soils using Helianthus annuus. Salt resistant plant beneficial bacterium (PBB) Pseudomonas libanensis TR1 and arbuscular mycorrhizal fungus (AMF) Claroideoglomus claroideum BEG210 were used. Inoculation of P. libanensis alone or in combination with C. claroideum significantly enhanced plant growth, changed physiological status (e.g. electrolyte leakage, chlorophyll, proline and malondialdehyde contents) as well as Ni and sodium (Na+) accumulation potential (e.g. uptake and translocation factor of Ni and Na+) of H. annuus under Ni and salinity stress either alone or in combination. These results revealed that bioaugmentation of microbial strains may serve as a preferred strategy for improving phytoremediation of metal-polluted saline soils.
- Serpentine bacteria influence metal translocation and bioconcentration of Brassica juncea and Ricinus communis grown in multi-metal polluted soilsPublication . Ma, Ying; Rajkumar, Mani; Rocha, Inês; Oliveira, Rui S.; Freitas, HelenaThe aim of this study was to assess the effects of inoculation of rhizosphere or endophytic bacteria (Psychrobacter sp. SRS8 and Pseudomonas sp. A3R3, respectively) isolated from a serpentine environment on the plant growth and the translocation and accumulation of Ni, Zn, and Fe by Brassica juncea and Ricinus communis on a multi-metal polluted serpentine soil (SS). Field collected SS was diluted to 0, 25, 50, and 75% with pristine soil in order to obtain a range of heavy metal concentrations and used in microcosm experiments. Regardless of inoculation with bacteria, the biomass of both plant species decreased with increase of the proportion of SS. Inoculation of plants with bacteria significantly increased the plant biomass and the heavy metal accumulation compared with non-inoculated control in the presence of different proportion of SS, which was attributed to the production of plant growth promoting and/or metal mobilizing metabolites by bacteria. However, SRS8 showed a maximum increase in the biomass of the test plants grown even in the treatment of 75% SS. In turn, A3R3 showed maximum effects on the accumulation of heavy metals in both plants. Regardless of inoculation of bacteria and proportion of SS, both plant species exhibited low values of bioconcentration factor (<1) for Ni and Fe. The inoculation of both bacterial strains significantly increased the translocation factor (TF) of Ni while decreasing the TF of Zn in both plant species. Besides this contrasting effect, the TFs of all metals were <1, indicating that all studied bacteria–plant combinations are suitable for phytostabilization. This study demonstrates that the bacterial isolates A3R3 and SRS8 improved the growth of B. juncea and R. communis in SS soils and have a great potential to be used as inoculants in phytostabilization scenarios of multi-metal contaminated soils.
- Inoculation with Metal-Mobilizing Plant-GrowthPromoting Rhizobacterium Bacillus sp. SC2b and Its Role in RhizoremediationPublication . Ma, Ying; Oliveira, Rui S.; Wu, Longhua; Luo, Yongming; Rajkumar, Mani; Rocha, Inês; Freitas, HelenaA plant growth-promoting bacterial (PGPB) strain SC2b was isolated from the rhizosphere of Sedum plumbizincicola grown in lead (Pb)/zinc (Zn) mine soils and characterized as Bacillus sp. based on (1) morphological and biochemical characteristics and (2) partial 16S ribosomal DNA sequencing analysis. Strain SC2b exhibited high levels of resistance to cadmium (Cd) (300 mg/L), Zn (730 mg/L), and Pb (1400 mg/L). This strain also showed various plant growth-promoting (PGP) features such as utilization of 1-aminocyclopropane-1-carboxylate, solubilization of phosphate, and production of indole-3-acetic acid and siderophore. The strain mobilized high concentration of heavy metals from soils and exhibited different biosorption capacity toward the tested metal ions. Strain SC2b was further assessed for PGP activity by phytagar assay with a model plant Brassica napus. Inoculation of SC2b increased the biomass and vigor index of B. napus. Considering such potential, a pot experiment was conducted to assess the effects of inoculating the metal-resistant PGPB SC2b on growth and uptake of Cd, Zn and Pb by S. plumbizincicola in metal-contaminated agricultural soils. Inoculation with SC2b elevated the shoot and root biomass and leaf chlorophyll content of S. plumbizincicola. Similarly, plants inoculated with SC2b demonstrated markedly higher Cd and Zn accumulation in the root and shoot system, indicating that SC2b enhanced Cd and Zn uptake by S. plumbizincicola through metal mobilization or plant-microbial mediated changes in chemical or biological soil properties. Data demonstrated that the PGPB Bacillus sp. SC2b might serve as a future biofertilizer and an effective metal mobilizing bioinoculant for rhizoremediation of metal polluted soils.
- Influence of mixtures of acenaphthylene and benzo[a]anthracene on their degradation by Pleurotus ostreatus in sandy soilPublication . Rocha, Inês; Pinto, Edgar; Ferreira, Isabel M. P. L. V. O.; Vieira Da Silva, Manuela; Oliveira, Rui S.Polycyclic aromatic hydrocarbons (PAHs) are a class of organic compounds commonly found as soil contaminants. Fungal degradation is considered as an environmentally friendly and cost-effective approach to remove PAHs from soil. Acenaphthylene (Ace) and Benzo[a]anthracene (BaA) are two PAHs that can coexist in soils; however, the influence of the presence of each other on their biodegradation has not been studied. The biodegradation of Ace and BaA, alone and in mixtures, by the white rot fungus Pleurotus ostreatus was studied in a sandy soil.
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