Rhizobacteria

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Cross section though a soybean (Glycine max 'Essex') root nodule: The rhizobacteria, Bradyrhizobium japonicum, colonizes the roots and establishes a nitrogen-fixing symbiosis. This high-magnification image shows part of a cell with single bacteroids within their host plant. In this image, endoplasmic reticulum, dictysome, and cell wall can be seen. Root-nodule01.jpg
Cross section though a soybean (Glycine max 'Essex') root nodule: The rhizobacteria, Bradyrhizobium japonicum , colonizes the roots and establishes a nitrogen-fixing symbiosis. This high-magnification image shows part of a cell with single bacteroids within their host plant. In this image, endoplasmic reticulum, dictysome, and cell wall can be seen.

Rhizobacteria are root-associated bacteria that can have a detrimental (parasitic varieties), neutral or beneficial effect on plant growth. The name comes from the Greek rhiza, meaning root. The term usually refers to bacteria that form symbiotic relationships with many plants (mutualism). Rhizobacteria are often referred to as plant growth-promoting rhizobacteria, or PGPRs. The term PGPRs was first used by Joseph W. Kloepper in the late 1970s and has become commonly used in scientific literature. [1]

Contents

Generally, about 2–5% of rhizosphere bacteria are PGPR. [2] They are an important group of microorganisms used in biofertilizer. Biofertilization accounts for about 65% of the nitrogen supply to crops worldwide.[ citation needed ] PGPRs have different relationships with different species of host plants. The two major classes of relationships are rhizospheric and endophytic. Rhizospheric relationships consist of the PGPRs that colonize the surface of the root, or superficial intercellular spaces of the host plant, often forming root nodules. The dominant species found in the rhizosphere is a microbe from the genus Azospirillum . [3] [ failed verification ] Endophytic relationships involve the PGPRs residing and growing within the host plant in the apoplastic space. [1]

Nitrogen fixation

Nitrogen fixation is one of the most beneficial processes performed by rhizobacteria. Nitrogen is a vital nutrient to plants and gaseous nitrogen (N2) is not available to them due to the high energy required to break the triple bonds between the two atoms. [4] Rhizobacteria, through nitrogen fixation, are able to convert gaseous nitrogen (N2) to ammonia (NH3) making it an available nutrient to the host plant which can support and enhance plant growth. The host plant provides the bacteria with amino acids so they do not need to assimilate ammonia. [5] The amino acids are then shuttled back to the plant with newly fixed nitrogen. Nitrogenase is an enzyme involved in nitrogen fixation and requires anaerobic conditions. Membranes within root nodules are able to provide these conditions. The rhizobacteria require oxygen to metabolize, so oxygen is provided by a hemoglobin protein called leghemoglobin which is produced within the nodules. [4] Legumes are well-known nitrogen-fixing crops and have been used for centuries in crop rotation to maintain the health of the soil.

Symbiotic relationships

The symbiotic relationship between rhizobacteria and their host plants is not without costs. For the plant to be able to benefit from the added available nutrients provided by the rhizobacteria, it needs to provide a place and the proper conditions for the rhizobacteria to live. Creating and maintaining root nodules for rhizobacteria can cost between 12–25% of the plant's total photosynthetic output. Legumes are often able to colonize early successional environments due to the unavailability of nutrients. Once colonized, though, the rhizobacteria make the soil surrounding the plant more nutrient rich, which in turn can lead to competition with other plants. The symbiotic relationship, in short, can lead to increased competition. [4]

PGPRs increase the availability of nutrients through the solubilization of unavailable forms of nutrients and by the production of siderophores which aids in the facilitating of nutrient transport. Phosphorus, a limiting nutrient for plant growth, can be plentiful in soil, but is most commonly found in insoluble forms. Organic acids and phosphotases released by rhizobacteria found in plant rhizospheres facilitate the conversion of insoluble forms of phosphorus to plant-available forms such as H2PO4−. PGPR bacteria include Pseudomonas putida , Azospirillum fluorescens , and Azospirillum lipoferum and notable nitrogen-fixing bacteria associated with legumes includes Allorhizobium, Azorhizobium, Bradyrhizobium, and Rhizobium. [5]

Though microbial inoculants can be beneficial for crops, they are not widely used in industrial agriculture, as large-scale application techniques have yet to become economically viable. A notable exception is the use of rhizobial inoculants for legumes such as peas. Inoculation with PGPRs ensures efficient nitrogen fixation, and they have been employed in North American agriculture for over 100 years.

Plant growth-promoting rhizobacteria

Plant growth-promoting rhizobacteria (PGPR) were first defined by Kloepper and Schroth [6] to be soil bacteria that colonize the roots of plants following inoculation onto seed and that enhance plant growth. [7] The following are implicit in the colonization process: ability to survive inoculation onto seed, to multiply in the spermosphere (region surrounding the seed) in response to seed exudates, to attach to the root surface, and to colonize the developing root system. [8] The ineffectiveness of PGPR in the field has often been attributed to their inability to colonize plant roots. [3] [9] A variety of bacterial traits and specific genes contribute to this process, but only a few have been identified. These include motility, chemotaxis to seed and root exudates, production of pili or fimbriae, production of specific cell surface components, ability to use specific components of root exudates, protein secretion, and quorum sensing. The generation of mutants altered in expression of these traits is aiding our understanding of the precise role each one plays in the colonization process. [10] [11]

Progress in the identification of new, previously uncharacterized genes is being made using nonbiased screening strategies that rely on gene fusion technologies. These strategies employ reporter transposons [12] and in vitro expression technology (IVET) [13] to detect genes expressed during colonization.

Using molecular markers such as green fluorescent protein or fluorescent antibodies, it is possible to monitor the location of individual rhizobacteria on the root using confocal laser scanning microscopy. [3] [14] [15] This approach has also been combined with an rRNA-targeting probe to monitor the metabolic activity of a rhizobacterial strain in the rhizosphere and showed that bacteria located at the root tip were most active. [16]

Mechanisms of action

PGPRs enhance plant growth by direct and indirect means, but the specific mechanisms involved have not all been well characterized. [8] Direct mechanisms of plant growth promotion by PGPRs can be demonstrated in the absence of plant pathogens or other rhizosphere microorganisms, while indirect mechanisms involve the ability of PGPRs to reduce the harmful effects of plant pathogens on crop yield. PGPRs have been reported to directly enhance plant growth by a variety of mechanisms: fixation of atmospheric nitrogen transferred to the plant, [17] production of siderophores that chelate iron and make it available to the plant root, solubilization of minerals such as phosphorus, and synthesis of phytohormones. [18] Direct enhancement of mineral uptake due to increases in specific ion fluxes at the root surface in the presence of PGPRs has also been reported. PGPR strains may use one or more of these mechanisms in the rhizosphere. Molecular approaches using microbial and plant mutants altered in their ability to synthesize or respond to specific phytohormones have increased understanding of the role of phytohormone synthesis as a direct mechanism of plant growth enhancement by PGPRs. [19] PGPR that synthesize auxins, gibberellins and kinetins or that interfere with plant ethylene synthesis have been identified. [20]

Development of PGPRs into biofertilisers and biopesticides could be a novel way of increasing crop yield and decreasing disease incidence, [21] whilst decreasing dependency on chemical pesticides and fertilisers which can often have harmful effects on the local ecology and environment. [22]

Pathogenic roles

Studies conducted on sugar beet crops found that some root-colonizing bacteria were deleterious rhizobacteria (DRB). Sugar beet seeds inoculated with DRB had reduced germination rates, root lesions, reduced root elongation, root distortions, increased fungi infection, and decreased plant growth. In one trial the sugar beet yield was reduced by 48%. [23]

Six strains of rhizobacteria have been identified as being DRB. The strains are in the genera Enterobacter , Klebsiella , Citrobacter , Flavobacterium , Achromobacter , and Arthrobacter . Due to a large number of taxonomic species yet to be described, complete characterization has not been possible as DRB are highly variable. [23]

The presence of PGPRs has proven to reduce and inhibit the colonization of DRB on sugar beet roots. Plots inoculated with PGPRs and DRBs had an increase in production of 39% while plots only treated with DRBs had a reduction in production of 30%. [23]

Biocontrol

Rhizobacteria are also able to control plant diseases that are caused by other bacteria and fungi. Disease is suppressed through induced systemic resistance and through the production of antifungal metabolites. Pseudomonas biocontrol strains have been genetically modified to improve plant growth and improve the disease resistance of agricultural crops. In agriculture, inoculant bacteria are often applied to the seed coat of seeds prior to being sown. Inoculated seeds are more likely to establish large enough rhizobacterial populations within the rhizosphere to produce notable beneficial effects on the crop. [1]

They can also combat pathogenic microbes in cattle. Different forage species regulate their own rhizosphere to varying degrees and favouring various microbes. Kyselková et al 2015 find planting forage species known to encourage native rhizobacteria retards the spread within the soil of antibiotic resistance genes of cow faeces bacteria. [24] [25]

Related Research Articles

<span class="mw-page-title-main">Rhizobia</span> Nitrogen fixing soil bacteria

Rhizobia are diazotrophic bacteria that fix nitrogen after becoming established inside the root nodules of legumes (Fabaceae). To express genes for nitrogen fixation, rhizobia require a plant host; they cannot independently fix nitrogen. In general, they are gram negative, motile, non-sporulating rods.

<i>Paenibacillus</i> Genus of bacteria

Paenibacillus is a genus of facultative anaerobic, endospore-forming bacteria, originally included within the genus Bacillus and then reclassified as a separate genus in 1993. Bacteria belonging to this genus have been detected in a variety of environments, such as: soil, water, rhizosphere, vegetable matter, forage and insect larvae, as well as clinical samples. The name reflects: Latin paene means almost, so the paenibacilli are literally "almost bacilli". The genus includes P. larvae, which causes American foulbrood in honeybees, P. polymyxa, which is capable of fixing nitrogen, so is used in agriculture and horticulture, the Paenibacillus sp. JDR-2 which is a rich source of chemical agents for biotechnology applications, and pattern-forming strains such as P. vortex and P. dendritiformis discovered in the early 90s, which develop complex colonies with intricate architectures as shown in the pictures:

<span class="mw-page-title-main">Rhizosphere</span> Region of soil or substrate comprising the root microbiome

The rhizosphere is the narrow region of soil or substrate that is directly influenced by root secretions and associated soil microorganisms known as the root microbiome. Soil pores in the rhizosphere can contain many bacteria and other microorganisms that feed on sloughed-off plant cells, termed rhizodeposition, and the proteins and sugars released by roots, termed root exudates. This symbiosis leads to more complex interactions, influencing plant growth and competition for resources. Much of the nutrient cycling and disease suppression by antibiotics required by plants occurs immediately adjacent to roots due to root exudates and metabolic products of symbiotic and pathogenic communities of microorganisms. The rhizosphere also provides space to produce allelochemicals to control neighbours and relatives.

Paenibacillus polymyxa, also known as Bacillus polymyxa, is a Gram-positive bacterium capable of fixing nitrogen. It is found in soil, plant tissues, marine sediments and hot springs. It may have a role in forest ecosystems and potential future applications as a biofertilizer and biocontrol agent in agriculture.

Pseudomonas chlororaphis is a bacterium used as a soil inoculant in agriculture and horticulture. It can act as a biocontrol agent against certain fungal plant pathogens via production of phenazine-type antibiotics. Based on 16S rRNA analysis, similar species have been placed in its group.

Microbial inoculants also known as soil inoculants or bioinoculants are agricultural amendments that use beneficial rhizosphericic or endophytic microbes to promote plant health. Many of the microbes involved form symbiotic relationships with the target crops where both parties benefit (mutualism). While microbial inoculants are applied to improve plant nutrition, they can also be used to promote plant growth by stimulating plant hormone production. Although bacterial and fungal inoculants are common, inoculation with archaea to promote plant growth is being increasingly studied.

<span class="mw-page-title-main">Biofertilizer</span> Substance with micro-organisms

A biofertilizer is a substance which contains living micro-organisms which, when applied to seeds, plant surfaces, or soil, colonize the rhizosphere or the interior of the plant and promotes growth by increasing the supply or availability of primary nutrients to the host plant. Biofertilizers add nutrients through the natural processes of nitrogen fixation, solubilizing phosphorus, and stimulating plant growth through the synthesis of growth-promoting substances. The micro-organisms in biofertilizers restore the soil's natural nutrient cycle and build soil organic matter. Through the use of biofertilizers, healthy plants can be grown, while enhancing the sustainability and the health of the soil. Biofertilizers can be expected to reduce the use of synthetic fertilizers and pesticides, but they are not yet able to replace their use. Since they play several roles, a preferred scientific term for such beneficial bacteria is "plant-growth promoting rhizobacteria" (PGPR).

Agricultural microbiology is a branch of microbiology dealing with plant-associated microbes and plant and animal diseases. It also deals with the microbiology of soil fertility, such as microbial degradation of organic matter and soil nutrient transformations.

<span class="mw-page-title-main">Phosphate solubilizing bacteria</span> Bacteria

Phosphate solubilizing bacteria (PSB) are beneficial bacteria capable of solubilizing inorganic phosphorus from insoluble compounds. P-solubilization ability of rhizosphere microorganisms is considered to be one of the most important traits associated with plant phosphate nutrition. It is generally accepted that the mechanism of mineral phosphate solubilization by PSB strains is associated with the release of low molecular weight organic acids, through which their hydroxyl and carboxyl groups chelate the cations [an ion that have positive charge on it.] bound to phosphate, thereby converting it into soluble forms. PSB have been introduced to the Agricultural community as phosphate Biofertilizer. Phosphorus (P) is one of the major essential macronutrients for plants and is applied to soil in the form of phosphate fertilizers. However, a large portion of soluble inorganic phosphate which is applied to the soil as chemical fertilizer is immobilized rapidly and becomes unavailable to plants. Currently, the main purpose in managing soil phosphorus is to optimize crop production and minimize P loss from soils. PSB have attracted the attention of agriculturists as soil inoculums to improve the plant growth and yield. When PSB is used with rock phosphate, it can save about 50% of the crop requirement of phosphatic fertilizer. The use of PSB as inoculants increases P uptake by plants. Simple inoculation of seeds with PSB gives crop yield responses equivalent to 30 kg P2O5 /ha or 50 percent of the need for phosphatic fertilizers. Alternatively, PSB can be applied through fertigation or in hydroponic operations. Many different strains of these bacteria have been identified as PSB, including Pantoea agglomerans (P5), Microbacterium laevaniformans (P7) and Pseudomonas putida (P13) strains are highly efficient insoluble phosphate solubilizers. Recently, researchers at Colorado State University demonstrated that a consortium of four bacteria, synergistically solubilize phosphorus at a much faster rate than any single strain alone. Mahamuni and Patil (2012) isolated four strains of phosphate solubilizing bacteria from sugarcane (VIMP01 and VIMP02) and sugar beet rhizosphere (VIMP03 and VIMP 04). Isolates were strains of Burkholderia named as VIMP01, VIMP02, VIMP03 and VIMP04. VIMP (Vasantdada Sugar Institute Isolate by Mahamuni and Patil) cultures were identified as Burkholderia cenocepacia strain VIMP01 (JQ867371), Burkholderia gladioli strain VIMP02 (JQ811557), Burkholderia gladioli strain VIMP03 (JQ867372) and Burkholderia species strain VIMP04 (JQ867373).

<span class="mw-page-title-main">2,4-Diacetylphloroglucinol</span> Chemical compound

2,4-Diacetylphloroglucinol or Phl is a natural phenol found in several bacteria:

Soil microbiology is the study of microorganisms in soil, their functions, and how they affect soil properties. It is believed that between two and four billion years ago, the first ancient bacteria and microorganisms came about on Earth's oceans. These bacteria could fix nitrogen, in time multiplied, and as a result released oxygen into the atmosphere. This led to more advanced microorganisms, which are important because they affect soil structure and fertility. Soil microorganisms can be classified as bacteria, actinomycetes, fungi, algae and protozoa. Each of these groups has characteristics that define them and their functions in soil.

A bioeffector is a viable microorganism or active natural compound which directly or indirectly affects plant performance (biofertilizer), and thus has the potential to reduce fertilizer and pesticide use in crop production.

<span class="mw-page-title-main">Root microbiome</span> Microbe community of plant roots

The root microbiome is the dynamic community of microorganisms associated with plant roots. Because they are rich in a variety of carbon compounds, plant roots provide unique environments for a diverse assemblage of soil microorganisms, including bacteria, fungi, and archaea. The microbial communities inside the root and in the rhizosphere are distinct from each other, and from the microbial communities of bulk soil, although there is some overlap in species composition.

A phytobiome consists of a plant (phyto) situated in its specific ecological area (biome), including its environment and the associated communities of organisms which inhabit it. These organisms include all macro- and micro-organisms living in, on, or around the plant including bacteria, archaea, fungi, protists, insects, animals, and other plants. The environment includes the soil, air, and climate. Examples of ecological areas are fields, rangelands, forests. Knowledge of the interactions within a phytobiome can be used to create tools for agriculture, crop management, increased health, preservation, productivity, and sustainability of cropping and forest systems.

Induced systemic resistance (ISR) is a resistance mechanism in plants that is activated by infection. Its mode of action does not depend on direct killing or inhibition of the invading pathogen, but rather on increasing physical or chemical barrier of the host plant. Like the Systemic Acquired Resistance (SAR) a plant can develop defenses against an invader such as a pathogen or parasite if an infection takes place. In contrast to SAR which is triggered by the accumulation of salicylic acid, ISR instead relies on signal transduction pathways activated by jasmonate and ethylene.

Markus Weinmann is an agricultural scientist specialising in the area of Plant Physiology at the University of Hohenheim, and ranks as one of the pioneers of Bioeffector-Research aimed at improving plant growth, vitality and disease resistance. He is also coordinator of field experiments in the EU-Biofector-Project.

<span class="mw-page-title-main">Mycorrhiza helper bacteria</span> Group of organisms

Mycorrhiza helper bacteria (MHB) are a group of organisms that form symbiotic associations with both ectomycorrhiza and arbuscular mycorrhiza. MHBs are diverse and belong to a wide variety of bacterial phyla including both Gram-negative and Gram-positive bacteria. Some of the most common MHBs observed in studies belong to the phylas Pseudomonas and Streptomyces. MHBs have been seen to have extremely specific interactions with their fungal hosts at times, but this specificity is lost with plants. MHBs enhance mycorrhizal function, growth, nutrient uptake to the fungus and plant, improve soil conductance, aid against certain pathogens, and help promote defense mechanisms. These bacteria are naturally present in the soil, and form these complex interactions with fungi as plant root development starts to take shape. The mechanisms through which these interactions take shape are not well-understood and needs further study.

Disease suppressive soils function to prevent the establishment of pathogens in the rhizosphere of plants. These soils develop through the establishment of beneficial microbes, known as plant growth-promoting rhizobacteria (PGPR) in the rhizosphere of plant roots. These mutualistic microbes function to increase plant health by fighting against harmful soil microbes either directly or indirectly. As beneficial bacteria occupy space around plant roots they outcompete harmful pathogens by releasing pathogenic suppressive metabolites.

<span class="mw-page-title-main">Sheath blight of rice</span> Fungal disease of rice

Rice-sheath blight is a disease caused by Rhizoctonia solani, a basidiomycete, that causes major limitations on rice production in India and other countries of Asia. It is also a problem in the southern US, where rice is also produced. It can decrease yield up to 50%, and reduce its quality. It causes lesions on the rice plant, and can also cause pre- and post-emergence seedling blight, banded leaf blight, panicle infection and spotted seed.

<span class="mw-page-title-main">Plant microbiome</span>

The plant microbiome, also known as the phytomicrobiome, plays roles in plant health and productivity and has received significant attention in recent years. The microbiome has been defined as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity".

References

  1. 1 2 3 Vessy, J. Kevin (August 2003). "Plant Growth Promoting Rhizobacteria as Biofertilizers". Plant and Soil. 255 (2): 571–586. doi:10.1023/A:1026037216893. ISSN   0032-079X. S2CID   37031212.
  2. ↑ Antoun H, Prevost D (2005). Ecology of plant growth promoting rhizobacteria. In: Siddiqui ZA (Eds.) PGPR: Biocontrol and Biofertilization, Springer, The Netherlands, pp. 2
  3. 1 2 3 Bloemberg, Guido V.; Lugtenberg, Ben J. J. (August 2001). "Molecular basis of plant growth promotion and biocontrol by rhizobacteria". Current Opinion in Plant Biology. 4 (4): 343–350. doi:10.1016/S1369-5266(00)0183-7. PMID   11418345.
  4. 1 2 3 Cain, Michael L.; Bowman, William D.; Hacker, Sally D. (2011). "Chapter 16: Change in Communities". Ecology. Sinauer Associates. pp.  359–362. ISBN   978-0-87893-445-4.
  5. 1 2 Willey, Joanne M.; Sherwood, Linda M.; Woolverton, Christopher J. (2011). "Chapter 29: Microorganisms in Terrestrial Ecosystems". Prescott's Microbiology. McGraw-Hill. pp. 703–706. ISBN   978-0-07-131367-4.
  6. ↑ Kloepper, Joseph W.; Schroth, Milton N. (1978). "Plant growth-promoting rhizobacteria on radishes" (PDF). Proceedings of the 4th International Conference on Plant Pathogenic Bacteria. Angers, France: Station de Pathologie Végétale et Phytobactériologie, INRA. 2: 879–882. Archived from the original (PDF) on 2014-07-14.
  7. ↑ Aziz, Z.F.A.; Saud, H.M.; Rahim, K.A.; Ahmed, O.H. (2012). "Variable responses on early development of shallot (Allium ascalonicum) and mustard (Brassica juncea) plants to Bacillus cereus inoculation". Malaysian Journal of Microbiology. 8 (1): 47–50.
  8. 1 2 Kloepper, Joseph W. (1993). "Plant growth-promoting rhizobacteria as biological control agents". In Metting, F. Blaine Jr. (ed.). Soil Microbial Ecology: Applications in Agricultural and Environmental Management. New York, USA: Marcel Dekker Inc. pp. 255–274. ISBN   978-0-8247-8737-0.
  9. ↑ Benizri, E.; Baudoin, E.; Guckert, A. (2001). "Root colonization by inoculated plant growth promoting rhizobacteria". Biocontrol Science and Technology. 11 (5): 557–574. doi:10.1080/09583150120076120. S2CID   83702938.
  10. ↑ Lugtenberg, Ben J. J.; Dekkers, Linda; Bloemberg, Guido V. (2001). "Molecular determinants of rhizosphere colonization by Pseudomonas" (PDF). Annual Review of Phytopathology. 39: 461–490. doi:10.1146/annurev.phyto.39.1.461. PMID   11701873. Archived from the original (PDF) on 2014-07-14.
  11. ↑ Persello-Cartieaux, F.; Nussaume, L.; Robaglia, C. (2003). "Tales from the underground: Molecular plant-rhizobacteria interactions". Plant, Cell & Environment. 26 (2): 189–199. doi: 10.1046/j.1365-3040.2003.00956.x .
  12. ↑ Roberts, Daniel P.; Yucel, Irem; Larkin, Robert P. (1998). "Genetic approaches for analysis and manipulation of rhizosphere colonization by bacterial biocontrol agents". In Boland, Greg J.; Kuykendall, L. David (eds.). Plant-Microbe interactions and Biological Control. Books in Soils, Plants, and the Environment. Vol. 63. New York, USA: Marcel Dekker Inc. pp. 415–431. ISBN   978-0-8247-0043-0.
  13. ↑ Rainey, Paul B. (1999). "Adaptation of Pseudomonas fluorescens to the plant rhizosphere" (PDF). Environmental Microbiology. 1 (3): 243–257. doi:10.1046/j.1462-2920.1999.00040.x. PMID   11207743.
  14. ↑ Bloemberg, Guido V.; Wijfjes, André H. M.; Lamers, Gerda E. M.; Stuurman, Nico; Lugtenberg, Ben J. J. (2000). "Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: New perspectives for studying microbial communities". Molecular Plant-Microbe Interactions. 13 (11): 1170–1176. doi: 10.1094/MPMI.2000.13.11.1170 . hdl: 1887/62882 . PMID   11059483.
  15. ↑ Sørensen, Jan; Jensen, Linda E.; Nybroe, Ole (2001). "Soil and rhizosphere as habitats for Pseudomonas inoculants: New knowledge on distribution, activity and physiological state derived from micro-scale and single-cell studies". Plant and Soil. 232 (1–2): 97–108. doi:10.1007/978-94-010-0566-1_10.
  16. ↑ Lübeck, Peter S.; Hansen, Michael; Sørensen, Jan (2000). "Simultaneous detection of the establishment of seed-inoculated Pseudomonas fluorescens strain DR54 and native soil bacteria on sugar beet root surfaces using fluorescence antibody and in situ hybridization techniques". FEMS Microbiology Ecology. 33 (1): 11–19. doi: 10.1111/j.1574-6941.2000.tb00721.x . PMID   10922498.
  17. ↑ Zakry, F.A.A.; Shamsuddin, Z.H.; Khairuddin, A.R.; Zakaria, Z.Z.; Anuar, A.R. (2012). "Inoculation of Bacillus sphaericus UPMB-10 to young oil palm and measurement of its uptake of fixed nitrogen using the 15N isotope dilution technique". Microbes and Environments. 27 (3): 257–262. doi:10.1264/jsme2.ME11309. ISSN   1342-6311. PMC   4036051 . PMID   22446306.
  18. ↑ Riaz, Umair; Murtaza, Ghulam; Anum, Wajiha; Samreen, Tayyaba; Sarfraz, Muhammad; Nazir, Muhammad Zulqernain (2021), Hakeem, Khalid Rehman; Dar, Gowhar Hamid; Mehmood, Mohammad Aneesul; Bhat, Rouf Ahmad (eds.), "Plant Growth-Promoting Rhizobacteria (PGPR) as Biofertilizers and Biopesticides", Microbiota and Biofertilizers: A Sustainable Continuum for Plant and Soil Health, Cham: Springer International Publishing, pp. 181–196, doi:10.1007/978-3-030-48771-3_11, ISBN   978-3-030-48771-3, S2CID   230587254 , retrieved 2022-03-23
  19. ↑ Glick, Bernard R. (1995). "The enhancement of plant growth by free-living bacteria". Canadian Journal of Microbiology. 41 (2): 109–117. doi:10.1139/m95-015. ISSN   0008-4166.
  20. ↑ Chaitanya, K. J.; Meenu, S. (2015). "Plant growth promoting Rhizobacteria (PGPR): a review », , vol. 5, no 2, , p. 108–119". E3 J. Agric.Res. Develop. 5 (2): 108.
  21. ↑ Vessey, J. Kevin (2003-08-01). "Plant growth promoting rhizobacteria as biofertilizers". Plant and Soil. 255 (2): 571–586. doi:10.1023/A:1026037216893. ISSN   1573-5036. S2CID   37031212.
  22. ↑ Muth, F.; Leonard, A. S. (2019-03-18). "A neonicotinoid pesticide impairs foraging, but not learning, in free-flying bumblebees". Scientific Reports. 9 (1): 4764. Bibcode:2019NatSR...9.4764M. doi:10.1038/s41598-019-39701-5. ISSN   2045-2322. PMC   6423345 . PMID   30886154.
  23. 1 2 3 Suslow, Trevor V.; Schroth, Milton N. (January 1982). "Role of Deleterious Rhizobacteria as Minor Pathogens in Reducing Crop Growth" (PDF). Phytopathology. 72 (1): 111–115. doi:10.1094/phyto-77-111. ISSN   0031-949X.
  24. ↑ He, Ya; Yuan, Qingbin; Mathieu, Jacques; Stadler, Lauren; Senehi, Naomi; Sun, Ruonan; Alvarez, Pedro J. J. (2020-02-19). "Antibiotic resistance genes from livestock waste: Occurrence, dissemination, and treatment". npj Clean Water . Nature Portfolio. 3 (1): 1–11. doi: 10.1038/s41545-020-0051-0 . ISSN   2059-7037. S2CID   211169969.(PJJA ORCID 0000-0002-6725-7199)
  25. ↑ Cycoń, Mariusz; Mrozik, Agnieszka; Piotrowska-Seget, Zofia (2019-03-08). "Antibiotics in the Soil Environment—Degradation and Their Impact on Microbial Activity and Diversity". Frontiers in Microbiology . Frontiers. 10: 338. doi: 10.3389/fmicb.2019.00338 . ISSN   1664-302X. PMC   6418018 . PMID   30906284.
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