Abstract
Actinobacteria is one of the largest phyla within the domain Bacteria. This phylum comprises more than 400 genera heterogeneously distributed in up to 50 families, 20 orders and 6 classes, being composed with very diverse groups of microorganisms. Members included within this phylum were recovered from a wide range of aquatic and terrestrial environments and also from a huge number of higher organisms, including plants. Actinobacteria inhabiting soils and plants are well known as producers of bioactive molecules and as biocontrol agents, possessing antimicrobial activities mostly against pathogenic fungi and/or bacteria. Moreover, some of them have the capacity to exert beneficial effects on plant growth and development via different plant growth-promoting mechanisms, i.e., phytohormones biosynthesis, siderophore production, and phosphate solubilization, among others. The available genomic data revealed that members belonging to this phylum have a huge potential as Plant Probiotic Actinobacteria. A plethora of studies reported the isolation and identification of plant endophytic actinobacteria possessing those features and also their performance under controlled conditions. However, few studies show the effects of the inoculation of these actinobacteria on real field conditions. In this chapter, we will provide an overview of the available data on the Actinobacteria displaying plant growth-promoting features, particularly in the ones that already had applications in agriculture. Together with a correct taxonomic classification, we will present evidence that the Plant Probiotic Actinobacteria should be considered as a source of bacterial candidates that will be important for a future sustainable agriculture.
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15.1 Introduction
The Actinobacteria is a phylum of Gram-positive bacteria and one of the largest taxonomic units within the domain Bacteria (Barka et al. 2015). The majority of the Actinobacteria are free-living organisms, being well known for their ubiquitous presence in soil and aquatic habitats and their contribution to organic material recycling. Between these bacteria, we found indeed some of the most well-known producers of antibiotics, exemplified by the genera Streptomyces, Micromonospora and Actinomadura (Raja and Prabakarana 2011). The Actinobacteria establishes close relationships with their environment and the organisms of their surroundings, with key molecular exchanges that allow their coexistence. Within the phylum, we found pathogenic bacteria for humans (Mycobacteria, Nocardia, or Tropheryma), for plants (Streptomyces scabiei, which cause scab in potatoes), and for animals (Corynebacterium, Mycobacteria). However, beneficial actinobacteria are also found for all these organisms, Bifidobacterium being well known for their implication in human and animal health, Pseudonocardia for the protection of ant’s gardens, or Frankia for their symbiotic relationship with actinorhizal plants. New studies on bacterial communities have shown that Actinobacteria composition is related to plant health (Wang et al. 2017), inducing a new interest in the study of Actinobacteria’s role as plant endophytes. This is clearly remarkable in the number of new species described from plant tissues in the last 10 years (Table 15.1), with more than ten new species published on the International Journal of Systematic and Evolutionary Microbiology only in the last 3 months (August–October 2018). High numbers of actinobacterial taxa found in healthy plant tissues have compelled us to think that these microorganisms have the capacity to improve plant health and could act as plant probiotics.
The FAO/WHO Expert Consultation Report defines Probiotics as “live microorganisms which when administered in adequate amounts confer a health benefit on the host” (Hill et al. 2014). Consequently, plant probiotics should be defined as “live microorganisms which when administered in adequate amounts confer a health benefit on the plant”. Between the actinobacteria, Frankia genus could be considered the first and most studied plant probiotic actinobacteria. This genus has been studied for more than a century due to its ability to fix atmospheric nitrogen, which is exchanged with the plants with which it establishes symbioses (Beijerinck 1901; Carro et al. 2015). Presence of Frankia strains has been also related to improvements in stress tolerance, as high salinity concentration (Ngom et al. 2016) or soil degradation (Diagne et al. 2013). Nevertheless, many other genera have been included in the list of Plant Probiotic Actinobacteria in the last years, exemplified by Streptomyces, which have been shown to improve plant vegetative growth and to induce and contribute to plant defense from pathogen attacks (Conn et al. 2008); by Micromonospora, which are able to improve plant growth and the tripartite symbioses with rhizobia in legumes (Carro 2010; Martínez-Hidalgo et al. 2014); or by Arthrobacter, which are able to increase iron-stress resistance (Sharma et al. 2016). Most of the actinobacteria tested as plant probiotic bacteria have been directly inoculated on plants, in most of the cases to evaluate the protection against some pathogenic microorganisms. However, contrary to other bacteria, many of them have not been tested for the general characteristic evaluated to determine a plant growth-promoting bacteria (PGPB): nitrogen fixation capacity, phosphate solubilization, production of plant hormones (IAA, ACC desaminase), etc. In this chapter, an overview of Actinobacteria known as plant growth promoters will be given, with emphasis on their taxonomic position and their use in agriculture.
15.2 Current Taxonomy of Actinobacteria: Classic and NGS-Based Classification
The taxonomic status of a strain, according to the polyphasic taxonomy, is determined by both phenotypic and genotypic characterization. A combination of chemotaxonomic analysis and other phenotypic features (tolerance tests, enzyme production, ability to metabolize carbon and nitrogen sources) together with other genetic traits of the taxon (16S rRNA phylogeny, GC content, DNA–DNA hybridization) was classically used for new actinobacteria species descriptions (Carro and Nouiuoi 2017). The use of multilocus sequences analyses (MLSA) greatly improved the relationships between these new isolates (Carro et al. 2012) and the upstream taxa, as exemplified by the analysis done by Adekambi et al. (2011). Lately, the new sequencing technologies developed and its availability for the vast majority of researchers have introduced new methods for phylogenomic reconstructions, allowing a better classification regarding higher taxa never seen before. Specifically, the works developed by Sen et al. (2014) for the class Actinobacteria and Nouioui et al. (2018c) for the whole phylum have greatly rearranged their respective status.
The phylum Actinobacteria was first described by Cavalier-Smith (2002) and include six classes: Acidimicrobiia (Norris 2012), Actinobacteria (Stackebrandt et al. 1997), Coriobacteriia (König 2012), Nitriliruptoria (Ludwig et al. 2012), Rubrobacteria (Suzuki 2012) and Thermoleophilia (Suzuki and Whitman 2012). From these classes, 450 genera are unequally distributed, the majority of them (418) being within the class Actinobacteria. Endophytic bacteria have been described only in the class Actinobacteria and in the class Rubrobacteria. This latter class just comprises one plant-associated species, Solirubrobacter phytolaccae (Wei et al. 2014).
After last reclassification based of whole-genome sequences (Nouioui et al. 2018c), the class Actinobacteria comprises 20 orders: Acidothermales, Actinomycetales, Bifidobacteriales, Catenulisporales, Corynebacteriales, Cryptosporangiales, Frankiales, Geodermatophilales, Glycomycetales, Jiangellales, Kineosporiales, Micrococcales, Micromonosporales, Nakamurellales, Nitriliruptorales, Propionibacteriales, Pseudonocardiales, Sporichthyales, Streptomycetales and Streptosporangiales. Most of these orders contain endophytic strains; only in six of them, no plant related strains have been isolated (Acidothermales, Actinomycetales, Bifidobacteriales, Catenulisporales, Nitriliruptorales and Sporichthyales). Strains belonging to those orders are related to human samples or extreme habitats. All the other orders contain genera in which some or most of their species have been described as plant endophytes (isolated from within the plant tissues). Among them, the most important genera of plant pathogens are mainly found in the order Corynebacteriales, including Corynebacterium, Nocardia, and Rhodococcus; in the order Micrococcales, including Clavibacter, Curtobacterium, Leifsonia, and Rathayibacter; and in the order Streptomycetales, including some species of the genus Streptomyces, such as the phytotoxin-producer S. scabies (Lozi 1994). Although several species of these genera have been found to be pathogenic, in most cases other species within the same genus have been described as nonpathogenic endophytes or even plant growth-promoting bacteria, i.e., the strain BMG51109 of Nocardia (Ghodhbane-Gtari et al. 2018) or the strain SK68 of Streptomyces (Damodharan et al. 2018). Although not an exact distribution between pathogen and PGPB could be established between the genera of Actinobacteria, some relationships could be observed mainly due to these double functions of some genera (Fig. 15.1). Most of the pathogens appear in genera from the family Microbacteriaceae of the order Micrococcales, while Frankiales, Jiangellales or Micromonosporales include mainly PGPB or asymptomatic endophytic strains.
15.3 Genomes Data Mining of PGP Traits on Actinobacteria
New technologies have encouraged the research of genes from plant endophytes related to their abilities for plant growth promotion, generating full sets of candidate genes to be further analyzed due to their potential. Trujillo et al. (2014) and Carro et al. (2018a) identified some of these genes in several species of the genus Micromonospora, including genes related to plant hormones production, phosphate solubilization, or siderophores production, among the most common ones, and also genes related to the biosynthesis of trehalases or other degrading enzymes (amylases, cellulases, chitinases, pectinases, and xylanases), among the most interesting ones for biotechnological applications.
Most of the plant endophyte genomes have been shown to harbor a whole set of genes for central carbohydrate metabolism that could be related to the utilization of root exudates as energy source (Kang et al. 2016). Other frequently found genes include the ones related to nutrient deficiencies, oxidative stress, drought tolerance, as well as secretion mechanisms and signaling (Trujillo et al. 2015). Genes related to biosynthesis pathways of plant growth modulators, such as auxins and cytokinins, are generally found in most plant probiotic bacteria, which combined with others related to degradation of ethylene through 1-amino-cyclopropane-1-carboxylic acid deaminase generate further improvements of plant status under stress conditions. Some genes that contribute to efficient colonization and competitiveness are also important in first steps of interactions (Francis et al. 2016).
Genome analysis has also put in evidence the importance of actinobacteria as secondary metabolites producers and its possible use in agriculture for biological control. The production of several peptides and antibiotics observed in actinobacteria probiotics could be used to defend the host plant against pathogens (Paterson et al. 2017; Remali et al. 2017). The mechanism of biocontrol also involved induction of plant defense response by, for example, the upregulation of PR10a, NPR1, PAL, and LOX2 genes in colonized plants by Streptomyces (Patel et al. 2018).
15.4 Applications of Plant Probiotic Actinobacteria in Agriculture
The members of the phylum Actinobacteria have a huge and well-appreciated range of biotechnological applications. As we have seen before, the metabolic potential and the biological significance of several groups of actinobacteria are well known, which are of paramount importance in the biotech industries, mostly related to biomedicine (Golinska et al. 2015; Barka et al. 2015; Passari et al. 2017). Actinobacteria associated with plants, namely endophytic actinobacteria, have been studied for its application in agriculture (Palaniyandi et al. 2013), mainly in biocontrol and suppression of plant diseases and, in some cases, in plant growth promotion (Ganapathy and Natesan 2018; Singh and Dubey 2018) (Table 15.2). However, studies showing the effects of Plant Probiotic Actinobacteria on crop yields are still scarce (Viaene et al. 2016; Araujo et al. 2017). Some of those works are enumerated in Table 15.3.
Among Actinobacteria, the streptomycetes are one of the most abundant bacterial groups in soils, accounting for up to 10% of the total microbiome (Janssen 2006). The genus Streptomyces is the most studied genus within the phylum Actinobacteria, not only due to its uncountable properties but also because of the versatility of the species within this genus (Viaene et al. 2016).
The vast majority of the studies about the potential of Streptomyces strains as plant growth promoters and biocontrollers present effects under in vitro controlled conditions due to its innate ability to produce secondary metabolites (including antibiotic and antimicrobial compounds). Strains belonging to different species of the genus Streptomyces isolated from wheat rhizosphere and root endosphere showed several activities, such as chitinase and phytase activities, as well as phosphorous solubilization. These strains are also able to produce different compounds, such as IAA, siderophores, organic acids and antifungal metabolites (Jog et al. 2014). Wheat plants in growth chamber (lab-controlled conditions) inoculated with Streptomyces strains showed higher plant biomass, number of lateral roots and branches, and nutritional content (essential elements) in comparison with uninoculated control plants (Jog et al. 2014).
In tomato plants, Palaniyandi et al. (2014) isolated a Streptomyces strain, called PGPA39, from an agricultural soil, which possess ACC deaminase, biosynthesize IAA and solubilize phosphate. This strain was also halotolerant. Spores of this strain were mixed in sterilized soil and sown with tomato plants, alleviating stress in those plants and showing higher plant biomass and root development than that of noninoculated salt-stressed tomato control plants.
As shown, there are several species and strains belonging to this genus that have plant growth potential, but there are few reports regarding studies showing improvements in crop yields under real field conditions (Viaene et al. 2016; Araujo et al. 2017) (Table 15.3).
Alekhya and Gopalakrishnan (2017) performed a screening of actinobacteria isolated from chickpea rhizosphere to find strains with antagonistic potential. Seven strains belonging to different species of the genus Streptomyces and displaying several PGP traits (broad spectrum antifungal activity, hydrolytic enzymes, IAA and HCN biosynthesis and siderophore production) were selected and tested under greenhouse conditions and also, in a field assay. Under greenhouse conditions, inoculated chickpea plants exhibit an increase in shoot weight (up to 84%), root weight (up to 57%), pod number (up to 102%) and pod weight (up to 84%). At harvest time, field assays also showed better performance of chickpea plants inoculated with the selected Streptomyces strains: seed number (up to 22%), stover yield (up to 86%), grain yield (up to 17%) and total dry matter (up to 51%).
Studies on grafted Vitis vinifera plants showed also the beneficial effects of Streptomyces strains under field real conditions (Alvarez-Pérez et al. 2017). In this work, several actinobacterial strains were isolated from young grapevine plants rhizosphere and endosphere. The isolates displayed in vitro antifungal activity, which was confirmed in field assays conducted in three experimental open-root field nurseries of grafted plants. The presence of phytopathogenic fungi affecting grafted Vitis plants was dramatically reduced (Alvarez-Pérez et al. 2017).
In cereals, there are also some examples of studies confirming the PGP potential of Streptomyces strains under field conditions. Yandigeri et al. (2012) isolated several Streptomyces strains from roots of 5 different native plants from India. Those isolates produce IAA, ammonia and siderophores. Three of these strains were tested in wheat plants in a field assay under drought conditions. Their findings revealed that the strains were drought-tolerant and improved seedling vigor after inoculation. At harvest time, wheat plants had higher biomass and there was a significative increase in grain yields.
With the aim of identifying good biocontrol agents, Palazzini and colleagues isolated several strains from wheat anthers and later identified one of them as a good biocontrol strain, Streptomyces sp RC87B (Palazzini et al. 2007). This strain presented antifungal activities, particularly against Fusarium graminearum sensu stricto under in vitro and in a greenhouse assay using a wheat cultivar that is susceptible to Fusarium infections. Ten years later, a study using the same strains confirmed that this potential can also be translated to field conditions. Wheat susceptible to Fusarium infection experienced a reduction of disease incidence (Palazzini et al. 2017).
Not only Streptomyces but also other actinobacterial genera, i.e., Micromonospora, Microbispora, Microbacterium, Actinoplanes, or Arthrobacter, were also tested alone or in combination with other bacterial members such as rhizobia or other actinobacteria, mostly under lab-controlled conditions or greenhouse assays, even that there are some of these studies that involved field trials.
Co-inoculation of leguminous plants with actinobacteria and rhizobial strains produced beneficial effects in those plants, increasing the nodule number, symbiotic efficiency and the plant biomass in most of the cases. Micromonospora strains, able to produce hydrolytic enzymes and IAA, alone and in combination with Ensifer (Sinorhizobium) strains produced significative increases in shoot and root dry weights and shoot C, N, P and K elements in Medicago sativa plants under in vitro and greenhouse conditions (Martínez-Hidalgo et al. 2014).
A study involving a set of field trials with soybean plants showed that the co-inoculation of Bradyrhizobium japonicum USDA110 with a strain of Streptomyces leads to an enhancement of nitrogen fixation and the production of a higher plant biomass and grain yield (Soe et al. 2012).
Misk and Franco (2011) co-inoculated two strains of Mesorhizobium ciceri and different biocontrol-tested Streptomyces spp. on chickpea plants under greenhouse conditions. Some of those Streptomyces strains suppressed the incidence of Phytophthora root rot disease and, in combination with both mesorhizobial strains, also enhanced vegetative growth. Interestingly, these authors also identified a non-streptomycete strain belonging to the genus Microbispora, which showed biocontrol and PGP traits; sadly, this strain was not tested in the greenhouse assays.
Interestingly, there is a study reporting the beneficial effects of a triple inoculation of three actinobacterial strains, closely related to the species Actinoplanes campanulatus, Micromonospora chalcea and Streptomyces spiralis, on cucumber plants affected with damping-off disease produced by the phytopathogenic oomycete Pythium. The three isolates produced the highest level of growth promotion when together (El-Tarabily et al. 2009). Moreover, all three actinomycete strains, alone and in combination, significantly increased root and shoot production in the presence or absence of Pythium aphanidermatum in comparison with the untreated control.
Arthrobacter is another genus that is cited frequently as potential plant growth promoter and as bioremediation agent in agriculture. Khan et al. (2018) identified a rhizospheric strain of Arthrobacter woluwensis, strain AK1, which showed ABA and IAA production under saline conditions. This halotolerant strain mitigated salt stress and promoted rice growth under in vitro conditions and also promoted soybean growth under greenhouse conditions.
In a search for phosphate solubilizers, Valetti et al. (2018) isolated an Arthobacter strain that significatively increased the yield of rapeseed crops when compared with the yield produced by the negative control plots (no fertilized and non-inoculated). Interestingly, the harvest index derived from the Arthrobacter sp. LRCP-11 is superior to the one derived from the negative control and fertilized uninoculated treatment.
Furthermore, there is a recent study discussing the potential role of the genus Arthrobacter in burned forests (Fernández-González et al. 2017). These authors performed a metagenomic analysis of the holm oak rhizosphere of undisturbed and burned oak forests. Actinobacteria was the most abundant phyla in both cases but is more abundant in the burned one. The genus Arthrobacter was one of the genera in burned rhizospheres, showing a significant increase in abundance with respect to other genera of Actinobacteria. Isolates from this genus displayed hydrolytic enzyme activities and IAA production and some of them lead to the significant increase of alfalfa and pepper vegetative growth under greenhouse conditions.
15.5 Conclusions and Futures Perspectives
The use of Actinobacteria as plant probiotics is still in a very early stage compared with the use and application of other PGP bacteria. However, the high number of new species described having a close relationship with plants, including endophytic and rhizosphere actinobacteria, as well as the importance of these microorganisms revealed by plant microbiomes, make them a very interesting alternative to solve agricultural problems. These microorganisms have an excellent potential for plant protection due to its ability to produce inhibitory compounds that will not allow the development of plant pathogens, as well as inducing the natural defense systems of the plants, even from an early stage of development. The sequencing and further analysis of complete or nearly complete genomes have also evidenced the potential of the Actinobacteria. Future studies will help in the discovery of new molecules implicated in plant–endophyte symbiotic interactions. The actinobacteria are also soil microorganisms, a feature that will help in their permanence for a long period of time in this unpleasant environment. Until now, the application of these microorganisms in real agricultural conditions has been limited; however, the limitations of the use of pesticides and chemical fertilizers in several worldwide countries and the global acceptance of the use of Plant Probiotic Bacteria as a “Green” alternative will encourage the use of these Plant Probiotic Actinobacteria in real crop production.
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Menendez, E., Carro, L. (2019). Actinobacteria and Their Role as Plant Probiotics. In: Giri, B., Prasad, R., Wu, QS., Varma, A. (eds) Biofertilizers for Sustainable Agriculture and Environment . Soil Biology, vol 55. Springer, Cham. https://doi.org/10.1007/978-3-030-18933-4_15
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