Sustainability is a significant challenge currently being faced by human beings. How can we nourish the ever-growing world population and at the same time offer viable soil for future crop production for the next generations? Agricultural ecosystems are fragile and excessive inputs, especially chemicals (nitrogen and phosphate fertilizers) and pesticides, which enable maximal yield, could work for a while, but plant survival is a tributary of soil health, which is, in turn, intimately linked to microbial diversity for nutrient turnover. It has been reported that excessive chemical inputs exert negative impacts on humans and environmental health (Glick, 2012). Moreover, with these incoming chemical inputs, the plant microbiome is modified and in accordance with hologenome theory, which outlines that microorganisms play a role in the evolution of animals and plants (Rosenberg et al., 2009), presumably, the evolution of plants and their associated symbiont microbiota (named holobiont) could be affected.

Plant microbiome are analogous to the gut microbiome: just as the gut microbiome plays a central role in human health (O'Hara and Shanahan, 2006), so too does the plant microbiome present the same properties in plant health. The microbiome is the entire microbial population inhabiting the plant with an extension to the rhizospheric microbiome, as there are important interactions between both (Rosenberg et al., 2009). Among these microbial populations, there are an important group named PGPR “Plant Growth Promoting Rhizobacteria” for those living in the rhizosphere, which ameliorate plant growth both directly and indirectly (Kloepper, 1978) as well as PGPB “Plant Growth Promoting Bacteria” including rhizospheric bacteria and those which are free-living in the soil or associated to plants in rhizoplane, phyllosphere and inside plants as endophytes (Bashan and De-Bashan, 2005). These microbes help plant growth by enhancing soil nutrient availability (Scagliola et al., 2016), the supply of phytohormones, and provide systemic resistance induction against phytopathogens. Thus, the employment of Plant Growth Promoting Bacteria (PGPB) is considered a promising alternative to conventional agricultural practices, in terms of chemical fertilizer and control of pathogenic agents (Bashan, 1998).

The use of Actinobacteria in agricultural practice has increased in recent years, due to their potential action as PGPR and their ubiquitous repartition in plants (Yadav et al., 2018). Actinobacteria are Gram positive bacteria with a high G+C content in their DNA, ranging from 51 to more than 70% (Ventura et al., 2007), well known for their metabolite production, mainly antibiotics (Saxena, 2014). They are present in the phyllosphere, endosphere (Lopez-Velasco et al., 2013), rhizosphere, and are free living in soil (Bulgarelli et al., 2013). In addition to their PGPB action, some other actinobacterial characteristics could encourage wider use as bioinoculant: many Actinobacteria, which generally represent an abundant proportion of soil microbiota, are particularly effective plant root system colonizers and by forming spores, they are able to endure unfavorable growth conditions (Alexander, 1977) and are more persistent in drought soils (Santos-Medellín et al., 2017). They play a critical role in organic matter recycling (Lacey, 1978) by increasing soil organic matter and nitrogen content along with essential macro and micro-elements, which in turn ameliorate plant growth, carbon metabolism, and allocation, and improve plant yield (AbdElgawad et al., 2020). Finally, their antagonistic and competitive characteristics permit them to colonize the rhizosphere with regards to other soil microorganisms (Bulgarelli et al., 2013). All the characteristics cited above designate Actinobacteria as an auspicious inoculant.

Many studies have proven the PGP action of the plant microbiome, but there is a gap between in vitro trials and efficiency in the field, particularly concerning their commercialization as a final bio-input product. The purpose of this review is to demonstrate the beneficial and protective impact of Actinobacterial on plant growth by highlighting the main direct or indirect PGPB traits. All genera of this important taxon were examined to identify their potential PGPB actions. On the other hand, the main impediments and future prospects of their use as biofertilizers are discussed.

According to Ludwig et al. (2012), in terms of the number and variety of identified species, the phylum Actinobacteria represents one of the largest taxonomic units among the 18 major lineages currently recognized within the domain Bacteria, including 5 subclasses, 6 orders, and 14 suborders. Its genomic diversity reflects its biodiversity which could have great biotechnological applications (Ventura et al., 2007). But an update based on 16S rDNA trees done by Gao and Gupta (2012), eliminated the taxonomic ranks of subclasses and suborders, elevating the former subclasses and suborders to the ranks of classes and orders, respectively. The phylum “Actinobacteria” is thus divided into six classes: Acidimicrobiia (01 order) (Norris, 2012), Actinobacteria (include 20 orders) after the classification based on the whole genome (Nouioui et al., 2018), Coriobacteriia (02 order) (Gupta et al., 2013), Nitriliruptoria (02 orders) (Ludwig et al., 2012), Rubrobacteria (01 order) (Suzuki, 2012), and Thermoleophilia (02 orders) (Suzuki and Whitman, 2012). Based on Actinobacteria classification (Parte et al., 2020) (consulted 01/01/2022), the cited classes above include 73 families and 443 genera which are unequally distributed. The majority of them (394) are within the class Actinobacteria (Table 1).

Actinobacteria present various and different lifestyles including plant pathogens (e.g., Streptomyces scabiei, S. acidiscabies, and S. turgidiscabies) (Wanner, 2006), mammalian pathogens (e.g., Mycobacterium spp., Nocardia spp., Corynebacterium spp., Tropheryma spp., and Propionibacterium spp.), plant commensals (Leifsonia spp.), soil inhabitants (Streptomyces spp.) as reported by Ventura et al. (2007), nitrogen-fixing symbionts (Frankia) (Franche et al., 2009), and gastrointestinal tract (GIT) inhabitants (Bifidobacterium spp.) (Ventura et al., 2007; Barka et al., 2016). It should be noticed that members of Actinobacteria class are associated with plants growing in different habitats as well as under extreme environments (Goudjal et al., 2013; Singh et al., 2016; Sahay et al., 2017).

Rhizospheric Actinobacteria are predominant in nature, with economic importance to humans because both agricultural and forest fields depend on their contributions to soil systems (Yadav et al., 2017). They possess diverse physiological and metabolic properties, like extracellular enzyme production and the formation of a wide variety of secondary metabolites (Schrempf, 2001). Rhizosphere harbors diverse actinobacterial species which have been further exploited for secondary metabolites (Geetanjali, 2016; Yadav et al., 2018). It has been reported by Berdy (2003), that microorganisms produced about 23,000 bioactive secondary metabolites, over 10,000 of these compounds are produced by Actinobacteria, which represent 45% of all discovered bioactive microbial metabolites and 80% if we only consider those compounds used in a practical way. Among Actinobacteria, Streptomyces species produced around 7,600 compounds, and these statistical evaluations should increase, perhaps not in an exponential way, but with the continuous growth of the number of new microbial metabolites.

The genus Streptomyces dominated actinobacterial strains isolated from soil, representing over 95% (Williams and Vickers, 1988). These actinobacterial strains are considered Streptomyces and Non-Streptomyces. Among the bioactive compounds produced by Actinobacteria, antibiotics, which initially confer them competitiveness are the most important in terms of biotechnological application as they produce the majority of the naturally occurring antibiotics (Barka et al., 2016). Other actinobacterial metabolites possess biotechnological applications, including in antifungal (Hoshino et al., 2004), bioherbicide/biopesticide (Waldron et al., 2001), antiparasitic (Burg et al., 1979), antiviral (Farmer and Suhadolnik, 1972), antitumor agent (Igarashi et al., 2007), immunostimulatory (de Reijke et al., 1997), and immunosuppressive (Uyeda et al., 2001) products.

The endophytic trait has been described mostly in the class Actinobacteria (Singh and Dubey, 2018), but with the advances of molecular identification tools, other endophytic candidates have been revealed so far, as for Thermoleophilia class, e.g., Solirubrobacter phytolaccae (Solirubrobacterales order) (Wei et al., 2014) and Patulibacter (Solirubrobacterales order) (Ferrando et al., 2012); for Rubrobacteria class e.g., Rubrobacteria genus (Rubrobacterales order) (Girija et al., 2018) and Coriobacteria class (Ren et al., 2018).

The fact that Actinobacteria could survive mesophilic but also for some candidates at thermophilic conditions reaching 60°C is an encouraging trait for its inocula use (Edwards, 1993), a fortiori they are considered as aridity–winners by Marasco et al. (2021) who stated that aridity changes composition and interactions of the plant-microbial community, this by modulating the distribution of aridity-tolerant (winners) and aridity-susceptible (losers) bacterial taxa, which is in favor of the former in a dry environment. There have also been reports that actinobacterial inoculation could not only protect plants from the deleterious effects of drought but also show significant increases in their measured physiological parameters (Chukwuneme et al., 2020). Furthermore, acidophilic Actinobacteria could play a major role in the inoculation of plants living in acidic soil (Bull, 2011). Many halotolerant Actinobacteria have been isolated from saline environments and have proven to be useful crop protective agents to plants in stressful conditions (Siddikee et al., 2010; Zhou et al., 2017; Qin et al., 2018). The extremophile character of some actinobacterial strains could be a valuable tool for rehabilitating degraded areas under extreme environmental conditions and they can enhance crop production under multiple conditions of stress, such as extreme temperatures, pH, salinity, and drought (Qin et al., 2011).

Bacterial strains are considered as PGPR if they can fulfill at least two of the three following criteria: aggressive colonization, plant growth stimulation, or biocontrol (Vessey, 2003). Globally, plant growth-promoting rhizobacteria (PGPR) are the rhizosphere bacteria that can enhance plant growth by a wide variety of mechanisms like phytohormones production, 1-Aminocyclopropane-1-carboxylate (ACC) deaminase production, induction of systemic resistance (ISR), phosphate solubilization, siderophore production, biological nitrogen fixation (BNF), rhizosphere engineering, quorum sensing (QS) signal interference and inhibition of biofilm formation, exhibiting antifungal activity, production of volatile organic compounds (VOCs), promoting beneficial plant-microbe symbioses, interference with pathogen toxin production, etc. (Bhattacharyya and Jha, 2012; Kumar and Singh, 2020). From a practical point of view, PGP-microbes could be used as biofertilizers by providing macro and micronutrients like biological nitrogen fixation (Vessey, 2003) and utilization of insoluble phosphorous (Chang and Yang, 2009), as biostimulants or phytostimulants by improving nutrient use and efficiency thanks to phytohormones production (Lugtenberg et al., 2002), as biocontronl by controlling plant pathogens using antibiotics or siderophores (Vessey, 2003), for rhizomediation by enhancing heavy metal solubility or decreasing the bioavailability of toxic compounds (Denton, 2007), and as biotisation agents by reducing chemical inputs in in vitro plant tissues culture (Diehdhiou et al., 2021). Regarding Actinobacteria, one of the major components of rhizosphere microbial populations, they showed a significant ecological role in soil nutrient cycling (Halder et al., 1991; Elliott and Lynch, 1995) as well as in plant growth-promoting activities (Merzaeva and Shirokikh, 2006), and numerous reports (Gomes et al., 2000; Sousa Cd et al., 2008; Goudjal et al., 2013; Kaur et al., 2013) are available on their potential as plant growth-promoting agents. To illustrate plant promoting ability among Actinobacteria phylum, we reviewed the 443 actinobacterial genera by associating each of them to term “plant growth promotion.” The most relevant results are reported in Table 1.

Among the mechanism of action, we will report below major processes of plant growth promotion related to Actinobacteria. But before, one should wonder if PGP traits, precisely, which one or how many should be accumulated to exert the maximum growth improvement of plants. For example, the most effective strain E108, identified as Curtobacterium flaccumfaciens, has increased barley growth up to 300% but has shown only two out of the six investigated plant growth promoting activities comparatively to two other strains, namely the Microbacterium natoriense strain E38 and Pseudomonas brassicacearum strain E8, which did not promote plant growth even though they showed many PGP traits (Cardinale et al., 2015).

From the reviewed information discussed above, it is clear that Actinobacteria possess some interesting characteristics, such as ubiquity, rhizosphere colonization ability (filamentous structure), competitiveness, the capacity to resist harsh conditions, in addition to high strength spores that allow them to survive for prolonged periods in soil and in storage containers in addition to high PGP activity and nutrient cycling capability (Jog et al., 2016). Actinobacteria have proven their value as PGPR and biocontrol agent, but few available commercial actinobacterial products are disposable. Among these commercial products, we could cite an active ingredient, Strptomyces lydicus WYEC108, which gave rise to multiple commercial products: “Actinovate^® AG” (Elliott et al., 2009), “Actinovate^® SP” and “Micro108^® soluble” for biocontrol; “Micro108^® Seed” and “Inoculant Action Iron^®” (produced by Naturalindustries) for biocontrol and plant growth promotion. Streptomyces violaceusniger strain YCED9 microbial agent was named “Thatch Control” for biocontrol (produced by Naturalindustries); S. griseoviridis strain K61 “Mycostop^®” for biocontrol (Suleman et al., 2002); Streptomyces saraceticus KH400 “YAN TEN Streptomyces saraceticus” for biocontrol (produced by Yanten). Metabolite Polyoxin D (produced by Streptomyces cacoi var. asoensis) named AFFIRM^WDG (produced by Chlearychemical) and “PH-D^® Fungicide” (produced by Arista-na) both used as a fungicide for turfgrass fungi. Some field trials tested the innocuity of actinobacterial bioinoculation as it was done for “Mycostop^®,” which was used for the control of Fusarium wilt of carnation and root rot disease of cucumber, and has been used in greenhouse production to protect flowers from pathogens (White et al., 1990). Likewise, Actinovate®, a biocontrol formulation of Streptomyces lydicus registered from AgBio in the United States of America, has been suggested for a wide range of environments ranging from greenhouses to field conditions, similarly, for Streptomyces lydicus WYEC 108 (MicroPlus®), which has been reported to possess disease suppression against powdery mildew and several root decay fungi (Solanki et al., 2016).

In general terms, “innovation” should include academic research, governmental institutions, industry, and civil society. Overall scientists have made an effort to develop eco-friendly and safe living organisms such as bio-intrant for ameliorating crop yield and protecting plants from pathogens, but these efforts will be infructuous if industry is not interested. Secondly, if governments do not establish legislation supervising the biotechnological application of PGPBs and facilitating interaction between “university” and “industry” (for example spin-off projects from a university or research and development department in industry) and finally if society in general and farmers, in particular, do not adhere to the use of bioinoculation (Etzkowitz and Zhou, 2017).

This assessment being established, much effort should be made before commercializing Actinobacteria or actinobacterial products for the development of sustainable agricultural solutions, beyond laboratory trials, including field assays to evaluate bioinoculant facing plant species, soil nature, and environmental conditions, which are unique for each ecosystem. It is crucial to evaluate bio-input safety and prevent the spread of antibioresistance.

There are important fields of investigation in developing the use of PGPB for ameliorating plant growth, alleviating plants stress, and enhancing plant resistance to pests. Among these PGPB, Actinobacteria (PGPA) are increasingly studied (Nimaichand et al., 2016). Sustainable agriculture is well integrated in the roadmap of industrialized and developing countries. The former to minimize negative impacts on atmospheric greenhouse gas (GHG) concentrations and water quality caused by N and P losses following high fertilization rates (Haygarth et al., 2013) along with minimizing pesticide impact on environmental and human health (Bernardes et al., 2015). The latter, because they practice low-input agriculture where fertilizers, pesticides, and agro-technical machinery are not widely available (too expensive) and where the application of putative inexpensive bioinoculants is a great challenge (Bashan, 1998). The reviewed literature cited above clearly demonstrates the high potential of Actinobacteria in ameliorating plant growth, whether acting directly or indirectly, and/or as fighting tools against phytopathogens. Furthermore, much valuable research has highlighted the beneficial effects of Actinobacteria PGPB actions on crop yield outlining that these Actinobacterial strains could be candidates as microbial fertilizers. Future studies will deal with the next steps in terms of exploring the effect of these microorganisms on plants under greenhouse conditions (semi-controlled conditions), and then under field conditions (different soil characteristics, environmental conditions, agricultural practices…), and primarily, which formulations of these bioinoculants should be selected: liquid, organic, inorganic, polymeric or encapsulated. This “secret art” formulation will ensure compatibility with routine field practices, should be easy to use, environment-friendly, and have long storage quality (Bashan et al., 2014). In addition to these crucial scientific and bioprocessing stages, registration and regulatory approval of the product should be initiated once the bioinoculant proved its efficacy (Backer et al., 2018). It is obvious that the gap between in vitro trials and marketable final products necessitates investment, time, and multidisciplinary skills (Bashan et al., 2014). North America is considered a leader for bioinoculant production in terms of generating revenue, followed by Europe, Asia-Pacific, South America, and finally to a lesser extent Africa (Soumare et al., 2020). Based on the fact that the global biofertilizer market will reach US$1.66 billion by 2022 (Timmusk et al., 2017), government and industries should be confident of a return on any investment. Overall, the major applications of bioinoculation have used BNF bacteria (especially rhizobia of about 79%), followed by phosphate solubilizing bacteria (~15%) while other inoculants including mycorrhizal products make up the remaining percentage (Research, 2014). Based on the Actinobacteria PGP traits described in this review, which are in addition to their competitiveness, ubiquity, and tremendous potential for metabolite production, this large taxonomic group worth a special attention even if it is not considered as a best candidate presently. Ultimately, it should play a key role in formulating multi-strain inoculants with synergistic actions for promoting sustainable agriculture.

All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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