Appl Microbiol Biotechnol DOI 10.1007/s00253-015-6660-8

MINI-REVIEW

Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology Parijat Kusari 1 & Souvik Kusari 2 & Michael Spiteller 2 & Oliver Kayser 1

Received: 26 March 2015 / Revised: 28 April 2015 / Accepted: 30 April 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Quorum sensing, the cell-to-cell communication system mediated by autoinducers, is responsible for regulation of virulence factors, infections, invasion, colonization, biofilm formation, and antibiotic resistance within bacterial populations. Concomitantly, quorum quenching is a process that involves attenuation of virulence factors by inhibiting or degrading quorum signaling autoinducers. Survival of endophytic microorganisms, commonly known as endophytes, in planta is a continuous mêlée with invading pathogens and pests. In order to survive in their microhabitats inside plants, endophytes have co-evolved to not only utilize an arsenal of biologically active defense compounds but also impede communication between invading pathogens. Such antivirulence strategies prevent pathogens from communicating with or recognizing each other and thus, colonizing plants. The quenching phenomena often involves microbial crosstalk within single or mixed population(s) vis-à-vis gene expression, and production/modulation of quenching enzymes coupled to various antagonistic and synergistic interactions. This concept is particularly interesting because it can be biotechnologically translated in the future to quorum inhibiting antivirulence therapies without triggering resistance in This manuscript is dedicated with best wishes to Professor Dr. Hartmut Laatsch on the occasion of his 69th birthday * Oliver Kayser [email protected] 1

Department of Biochemical and Chemical Engineering, Chair of Technical Biochemistry, TU Dortmund, Emil-Figge-Str. 66, 44227 Dortmund, Germany

2

Institute of Environmental Research (INFU), Department of Chemistry and Chemical Biology, Chair of Environmental Chemistry and Analytical Chemistry, TU Dortmund, Otto-Hahn-Str. 6, 44221 Dortmund, Germany

bacteria, which is currently a major problem worldwide that cannot be tackled only with antimicrobial therapies. In this mini-review, we highlight the quorum quenching capacity of endophytes with respect to attenuation of virulence factors and aiding in plant defense response. Further, benefits and potential challenges of using such systems in biotechnology are discussed. Keywords Quorum sensing . Quorum quenching . Endophytes . Virulencefactors . Autoinducer . Drugresistance

Introduction Being one of the intensively investigated and pursued topics of research, quorum sensing as a phenomenon has gained importance in the fields of bacterial pathogenesis, colonization, invasion, antibiotic resistance, and emerging diseases (Claessen et al. 2014). Quorum sensing implies a cell-to-cell communication system within single or mixed microbial populations (Cornforth et al. 2014). Such signaling systems enable the microorganisms to detect the nearest microbial cell in a community for modulating their population densities, synergistic and antagonistic interactions, gene expressions, and metabolite trafficking. Generally, such communication systems are well established within bacteria, but different unicellular and filamentous fungal species have also shown to perform Bquorum sensing^-like functions. Moreover, several plants are also known to produce metabolites that mimic quorum sensing signaling molecules (Hartmann et al. 2014). Therefore, quorum sensing signaling is not only a phenomenon enabling two different microbes to communicate, rather it symbolizes a more complicated interactive state involving competing ecological niches comprising of bacterial, fungal, and plant species. The understanding of such dynamic

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signaling mechanisms requires an interpretation of the complete ecological niche, nonexistent in single species. Thus far, comprehensive elucidation of gene expression, virulence, and attenuation of virulence factors is a complicated issue that results in development of resistance of pathogens to bioactive secondary metabolites. The phenomenon for attenuation of virulence factors that lead to quorum sensing, commonly known as quorum quenching, represents an emerging field of research (Hong et al. 2012). In the recent years, microbial interactions with other microbes and with plants have garnered immense importance in biotechnology and agriculture research. Taking the overall plant-microbe interactions into account, a unique group of microorganisms called endophytes, which are either fungi or bacteria that reside mutualistically within the internal tissues of host plants, have been extensively studied with regard to the capacity in maintaining bi- and tripartite associations with host plants and associated microorganisms (Kusari et al. 2013). The endeavor of endophytic microorganisms to maintain colonization in a particular habitat and resist various environmental interferences lays a scientific handle to investigate a cascade of signaling systems. For example, studying endophytes using co-culture systems, their antagonistic and synergistic associations, plant defense responses against host specific or generalized pathogens, production of cryptic and novel metabolites by endophytes, ecological implications of endophyte crosstalk with host plant, and associated microbial community constitute some of the major functional traits of endophytes in the current research scenario (Brader et al. 2014; Higgins et al. 2014; Kusari et al. 2014a; b; c; d; Moebius et al. 2014; Aly et al. 2013). It is compelling that endophytes co-evolve with host plants to recognize a plethora of signaling molecules, particularly those of invading pathogens, and concurrently develop strategies to maintain colonization within plant tissues. One such endophytic functional trait encompasses quenching of pathogen quorum molecules. Herein, we highlight the current scenario of quorum quenching systems primarily involving endophytic microorganisms with a focus on their associations, attenuation of virulence factors, and inhibition strategies. Endophytic production or degradation of quorum autoinducers, subsequent benefits, and potential challenges associated with such systems effecting overall plant fitness are also discussed.

Short perspective on quorum sensing The concept of cell-to-cell communication, also known as quorum sensing, by signaling molecules called autoinducers started with the discovery of N-(3-oxohexanoyl)- L homoserine lactone in Vibrio fischeri (Nealson and Hastings 1979). Generally, the quorum sensing mechanisms involving N-acyl-L-homoserine lactones (AHLs) are observed in Gram-

negative bacteria and oligopeptide autoinducers in Grampositive bacterial species (Dichschat 2010; Miller and Bassler 2001). Beyond these universal autoinducers, existence of other signaling molecules such as diffusible signal factors, autoinducers-2 and −3, and quinolone signals have been found in different bacterial populations (LaSarre and Federle 2013; Galloway et al. 2011; Hosni et al. 2011). The AHL autoinducers are responsible for various biological activities like swarming motility, biofilm formation, regulation of virulence genes, and antibiotic production in a wide range of Gram-negative bacterial species (Dong et al. 2000). Since the initial breakthrough in 1979, several autoinducers and quorum sensing mechanisms have been recognized in different microbial systems across varied ecological niches. Interestingly, several unicellular and filamentous fungal species have been recognized to perform quorum sensing (Leonhardt et al. 2015; Safari et al. 2014; Sorrentino et al. 2010; Hogan 2006; Chen et al. 2004). Plant systems form an important habitat for microbes and show deep involvement with surrounding microbial associates in antagonistic and synergistic manner. Therefore, co-evolution of plants with associated microbiome lead to production of signaling compounds that mimic the microbial autoinducers (Hartmann et al. 2014; Teplitski et al. 2011). Nevertheless, such associations often rely on the utilization of multispecies crosstalk that makes it even more complicated to understand and interpret the trafficking of signaling molecules at the organismal interfaces. Cornforth et al. (2014) have profoundly analyzed such complexities in Pseudomonas aeruginosa via simulation models to calculate the dynamics of signaling molecules in mixed microbial populations. In nature, microbes and plants are constantly in association either with each other or with associated microflora and macroflora. Therefore, interpreting the population dynamics, gene expression and corresponding metabolite production involving microbe-microbe and plantmicrobe quorum sensing phenomena still remains a challenge.

Inhibition of quorum sensing (quorum quenching) Quorum quenching is defined as a process that inhibits quorum sensing signaling across microbial populations by targeting virulence factors (Kusari et al. 2014a; Hosni et al. 2011). The degradation and/or disruption of autoinducers in a variety of bacterial species utilizing quenching enzymes were recently summarized by Hong et al. (2012). Recognition and subsequent disruption of quorum sensing molecules have been demonstrated by plants. Overexpression of different phytohormones like auxins and cytokinins, physiological changes, expression of genes involved in defense responses, and formation of reactive oxygen species are the major counter strategies studied in different plant systems to attenuate the virulent autoinducers of quorum responses (Bai et al. 2012;

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Schenk et al. 2012; Ortíz-Castro et al. 2008; von Rad et al. 2008). Extracts from different medicinal plants and herbs (Koh and Tham 2011; Adonizio et al. 2006), selected plant tissues including root and fruits (Kim and Park 2013; Harjai et al. 2010; Bodini et al. 2009; Truchado et al. 2009; Girennavar et al. 2008; Zhu and Sun 2008), animal proteins (Teplitski et al. 2011), bioactive natural products from plants (LaSarre and Federle 2013), natural products from marine ecosystems (Natrah et al. 2011a, b; Tait et al. 2010; Skindersoe et al. 2008), different oils (Khan et al. 2009), and even food products (Jakobsen et al. 2012; Vattem et al. 2007) exhibit quorum quenching efficacies. Therefore, a broad spectrum of bioactive natural products originating from diverse sources is effective against quorum responses (Fig. 1). The biotechnological applications of targeting drug resistance using natural products can be further exploited if certain factors like autoinducer triggering factors, production and release of signals, reception of proper signals, and multiple signaling complexities are considered. Although the different nutritional conditions and natural selection pressures might change with different habitat and involvement of multiple partners, attempts can still be made for reduction of drug resistance and virulence in pathogenic bacterial communities. Several attempts to encounter quorum responses have already been made in various biotechnological areas involving agriculture (Zhou et al. 2008), pharmacology (Estrela and Abraham 2010; Givskov et al. 1996), biofouling (Callow and Callow 2011; Molino et al. 2009; Yeon et al. 2009), and marine ecosystems (Natrah et al. 2011a, b; Skindersoe et al. 2008). Therefore, investigations on microbial communities demonstrating quorum quenching will continue to serve as a promising field of research.

Endophytic quorum sensing systems for host plant colonization Plants from varied genera are known to produce AHL mimic compounds (Perez-Montano et al. 2013) for defense mechanisms against pathogens and interaction with associated microbial communities, both within as well as outside the plant tissues. Quorum mimicking AHLs are produced and released in the near vicinity by various plant species ranging from seedlings to a mature plant (Teplitski et al. 2011). Endophytes forming an integral part of plant systems are often found aiding in plant defense responses by quorum inhibiting mechanisms. Interestingly however, endophytes are often found to have quorum sensing systems that allow them to maintain their own colonization in host plants and counter phytopathogens. For example, strain PsJNT is reported to establish endophytic associations with various plants and known to improve plant rooting system with enhanced vascular systems, increase amounts of chlorophyll and phytohormones, and provide

resistance to plant pathogens. Interestingly, strain PsJNT was found to produce quorum autoinducer 3-hydroxy-C8homoserine lactone (Sessitsch et al. 2005). Furthermore, endophytic Serratia plymuthica with immense biocontrol potential was found to contain high amount of homoserine lactone (HSL) namely, C4-HSL, C5-HSL, C6-HSL, C7-HSL, C8HSL, 3-oxo derivatives (3-oxo-C6-HSL, 3-oxo-C7-HSL, 3oxo-C8-HSL), and 3-hydroxy derivatives (3-hydroxy-C6HSL, 3-hydroxy-C8-HSL). These AHL molecules were due to two quorum sensing systems in S. plymuthica (Liu et al. 2011). The genome sequence of endophytic Gluconacetobacter diazotrophicus PAL5 harbored in Saccharum officinarum (commonly known as sugarcane) revealed the presence of quorum sensing systems and identification of eight AHLs viz.C6, C8, C10, C12, and C14-HSL (Nieto-Penalver et al. 2012). A recent report from Dourado et al. (2013) exemplified the use of quorum sensing molecules for Methylobacterium (known to exhibit endophytic lifestyle) interactions with plants. A series of genes were up- and down regulated in Methylobacterium and host plant simultaneously enabling colonization and symbiotic associations, showing the dependency of plant-endophyte associations on quorum sensing systems. Further, the olive plant epiphyte (Pantoea agglomerans) and endophyte (Erwinia toletana) associated with olive knot disease were monitored to release signals similar to AHLs (Hosni et al. 2011). Such chemical signaling modulated the virulence of pathogen Pseudomonas savastanoi pv. savastanoi responsible for olive knot. This work is an example of tripartite interactions between plant and associated microorganisms. Rhizosphere bacteria are long known to enhance yields of plants by nitrogen fixation, production of siderophores and phytohormone, reduce plant stress, induce systemic resistance, and possess capacity to attenuate plant pathogenic signals (Liu et al. 2012). Therefore, possessing quorum sensing systems and autoinducers might enable the endophytic isolates to communicate with other associated endophytes as well as the host plant, thereby maintaining symbiotic association and colonization within the internal tissues of plants. Admittedly, there is a dearth of information on such systems, which need to be studied in depth to look for the plausible plant physiological changes and defense responses such as release of ethylene, salicylic acid, and defense proteins during the initial stages of colonization.

Quorum quenching by endophytes Recent advances on endophytes displaying quorum responses to target virulence factors and pathogenicity represent an emerging field of research. Figure 2 schematically depicts the quorum responses with respect to plant, endophyte, and pathogen. Quenching or degradation of autoinducers is generally mediated by two quorum quenching enzymes namely,

Appl Microbiol Biotechnol Fig. 1 Overview of quorum quenching natural products from diversified sources and the associated challenges and benefits

lactonase and acylase (Hong et al. 2012). The AHL autoinducers found in a variety of bacterial pathogens involved in regulation of virulent gene expressions are mainly formed of a common homoserine lactone moiety with variations in length of acyl chain. The basic idea is to utilize AHL lactonase (quorum quenching enzyme), which hydrolyzes the lactone bonds making it incapable of binding to target transcriptional regulators and enhance resistance against pathogen infections mediated by AHL autoinducers. Research reports suggest the use of AHL lactonase for inactivation of virulence in plant pathogen Erwinia carotovora by expression of aiiA gene encoding for AHL inactivation (Dong et al. 2000, 2001). The aiiA gene mediated targeting of pathogenic signals is reported in a variety of soil bacteria, Bacillus sp., subspecies of Bacillus thuringiensis (Ulrich 2004; Lee et al. 2002). Similar concept of AHL lactonase mediated quorum quenching has been recently reported from endophytic bacterial species of Enterobacter isolated from a woody plant climber Ventilago madraspatana (commonly known as red creeper) (Rajesh and Rai 2014a). The aiiA homologue gene was successfully amplified in endophytic Enterobacter sp., namely Enterobacter asburiae VT65, Enterobacter aerogenes VT66, and Enterobacter ludwigii VT70 indicating the presence of AHL lactonase. Further, the putative tertiary structure of endophytic AHL lactonase was determined. Endophytic bacteria colonizing Pterocarpus santalinus L. plant (otherwise known as red sandalwood), was also found to carry aiiA homologue gene containing a conserved zinc binding motif, effective against C4-HSL and 3-oxo-C12-HSL (Rajesh and Rai 2014b). Interestingly, the cell-free lysates of the endophytic bacterial isolates were also found to inhibit biofilm formation

in P. aeruginosa PAO1, a known human pathogenic strain causing chronic infections. Such reports on endophytes indicate the possibility of utilizing genetically transformed endophytes against virulence factors of generalized or plant pathogens. Attempts made in this direction could enhance the possibility of aiding in host plant defense responses by countering or suppressing phytopathogen virulence factors. Cho et al. (2007) have shown the transformation of aiiA gene from B. thuringiensis into endophyte Burkholderia sp. strain KJ006 to attenuate the seedling and grain rot infection caused by Burkholderia glumae in rice. Apart from lactonase, AHLacylase activity was also reported from endophytic actinomycete Streptomyces LPC029, which could suppress the soft rot infection by Pectobacterium carotovorum ssp. carotovorum on potato (Chankhamhaengdecha et al. 2013). This shows that endophytic microorganisms can maintain colonization in host plants and aid in plant defense responses in particular ecological niches. It is often seen that similar endophytic bacterial species are harbored in different host plants. In the near future, engineered endophytic isolates could also be used against host plant pathogens having similar infection symptoms, hinting toward a large-scale application of endophytes as biocontrol tools in agriculture. Furthermore, emerging techniques like matrix-assisted laser desorption ionization imaging highresolution mass spectrometry (MALDI-imaging-HRMS) have been employed to quantify and visualize the suppression of C6, C8, C10, and 3-oxo-C10 HSL by endophytic bacterial isolates of Cannabis sativa L. (Kusari et al. 2014a). These techniques provide better insights into endophytic quenching phenomenon with spatial and temporal visualization of distribution of autoinducers in a microbial colony. Therefore, such

Appl Microbiol Biotechnol Fig. 2 Schematic representation of quorum responses with respect to plant, endophyte, and pathogens. QS, quorum sensing; QQ, quorum quenching; AI, autoinducer; AHL, N-acyl-Lhomoserine lactone

techniques can be employed to monitor microbe-microbe interactions with response to release, uptake, and degradation of quorum sensing signals. Endophytic fungal isolates have been rigorously exploited for production of bioactive natural products with potential pharmaceutical and agricultural applications (Kusari et al. 2014c). With respect to quorum quenching efficacies, endophytic fungal isolates have been reported to produce natural products, even novel metabolites that could attenuate the autoinducers. For example, endophytic fungi Fusarium graminearum and Lasiodiplodia sp., harbored in Ventilago madraspatana (commonly known as red creeper), exhibited quorum sensing inhibition against biosensor Chromobacterium violaceum (Rajesh and Rai 2013). Figueroa et al. (2014) isolated an endophytic fungus Penicillium restrictum, from the stems of Silybum marianum (the medicinal plant, milk thistle) producing a series of polyhydroxyanthraquinones (five of them were novel compounds) with potent antivirulence activity against

methicillin-resistant Staphylococcus aureus. Interestingly, desorption electrospray ionization−mass spectrometry (DESIMS) showed the accumulation of quorum quenching polyhydroxyanthraquinones at the surface of the fungal mycelia. Accumulation of metabolites around the periphery of fungal mycelia is indicative of utilization as transport molecule or signaling molecule that can easily come in contact with associated pathogens or endophytes. Further, flavipesins A isolated from a mangrove plant’s (Acanthus ilicifolius) endophytic fungus Aspergillus flavipes AIL8 exhibited antibiofilm activity against S. aureus (Bai et al. 2014). S. aureus is known to cause fatal human infections due to its multidrug resistance capacity. Multidrug resistance is presently a huge problem worldwide and antivirulence strategy against such drug resistance (Clatworthy et al. 2007), both within clinical and ecological settings, are currently a major focus of research. Therefore, natural products targeting virulence factors mainly quorum sensing signaling autoinducers, instead of microbial growth, could serve as potential drug molecules to counter

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such infections. Applications in pharmaceutical and clinical sectors for drug molecules would require consistent biotechnologically feasible production of natural products from endophytes. Recently, endophytic fungal isolates from a marine ecosystem (reef organisms) was also exploited for quorum inhibiting efficacies (Martín-Rodríguez et al. 2014). Four endophytic fungal isolates (marine endophytes) belonging to Sarocladium, Fusarium, Epicoccum, and Khuskia genera were found to be positive against quorum autoinducers. This shows that endophytic fungi can serve as reservoirs of quorum inhibiting enzymes and could be exploited for understanding the regulation and production of bioactive secondary metabolites for applications in pharmaceutical sectors.

Outlook Endophytes are capable of maintaining mutualistic associations with their host plants, which often lead to co-evolution of certain functional traits such as production of bioactive natural products, aiding in plant defense responses by either production of quorum inhibiting enzymes or possessing own quorum signaling chemicals. However, during their coexistence with host plants, endophytes encounter invasion by a plethora of specific and generalist pathogens. Therefore, in order to survive in their ecological niches, endophytes might evolve additional defense strategies that prevent the pathogens from developing resistance against endophytic and host plant defense compounds, and thus, sustain their survival within host plants (Table 1). Furthermore, endophytes might contribute to plant fitness and higher yield of secondary natural products in callus and cell suspension cultures. Although there are reports of novel secondary metabolites that can target the virulence in multidrug resistance bacterial pathogens, the main difficulty lies in constant gene expression and production of natural products during repeated subculturing outside host plants, which could be used for maintaining callus culture and impacting biosynthetic routes. Moreover, the complexity of natural conditions encompassing nutrition, host plant environment, soil, climate conditions and pH, and the

Table 1

constant associated interactions within plant tissues could severely affect the efficacy and triggering of endophytic production of quenching compounds in vitro. Another obstacle is to understand the host plant gene regulations, if any, which support endophytes to fight collectively against invading phytopathogens. Such problems might be addressed with suitably designed co-culture systems and proper analysis of all target functional genes. On the one hand, supplementing laboratory biotech culture conditions with different carbon, nitrogen, and other essential elements and salts to modify the extracellular nutritional conditions could be a possible way forward for optimal production. On the other hand, trying to grow potent endophytes on nutrient deficient conditions will enable understanding of production of quorum inhibiting compounds in populations with competition for nutrients. Understanding of optimal nutritional environment would enable better upscaling of bioactive quenching natural products produced by endophytes and help in biotechnological quorum inhibiting therapies targeting drug resistance in human and plant pathogenic strains. The release of quorum autoinducers in any habitat is also dependent on bacterial population density in an ecological niche. One of the prime factors is to know the exact microbial population in a system to differentiate between autoinducer producers and Bcheater^ microbes that do not produce any quorum signaling chemicals (Sandoz et al. 2007). This would then make it easier to target the specific microbial community with capacity to release virulence factors. Furthermore, the use of engineered endophytes with AHL lactonase gene could also be utilized for suppressing pathogenicity in an agricultural setup. This strategy could be employed on crop plants with common pathogen symptoms and autoinducers for infections. It can, therefore, be employed in the future for applications in agriculture to prevent mass destruction of crops and medicinal plants under field conditions. Furthermore, bacteria with yet unknown functions vis-à-vis quorum sensing signaling can be investigated using transformed endophytes with aiiA gene as a marker to identify the individual and synergistic roles of autoinducers. Admittedly, all the present strategies and attempts reported for endophyte-mediated quorum inhibition

Summary of the overall objectives and challenges associated with endophytic quorum quenching

Objectives

Challenges

• Plant fitness benefits • Higher yield of secondary metabolites • Survival inside host plants • Target virulence factors • Prevent pathogens from developing resistance to defensive compounds • Quorum inhibiting therapies

• Repeated subculturing of endophytes outside host plants influences the production of natural products • Difference of nutrition, host plant environment, soil, climate conditions pH, and the constant associated interactions within plant could affect the efficacy • Understanding host plant gene expression and regulation • Microbial population density • Differentiate between actual producer and cheater microorganisms in any ecological niche • Multiple signaling systems in microbial populations • Understanding the exact role of single and combined autoinducers in any natural habitat

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processes and colonization revolve around single or two microorganisms and host plants. It is desirable to understand the exact role of autoinducers and triggering factors in mixed microbial populations, which exist in natural settings that might result in simultaneous release of multiple autoinducers. Release of any particular autoinducer or mixed autoinducers might interfere with other signaling systems and inactivate the beneficial quorum quenching enzymes. Therefore, employing multiple quorum attenuating systems against targeted virulence factors seems to be an effective remedy. Interestingly, multiple quorum quenching strategies are persistent in nature. The major impediment lies in underlining the exact role of such combined quorum inhibition signals. Acknowledgments We gratefully acknowledge the Ministry of Innovation, Science, Research, and Technology of the State of North RhineWestphalia, Germany and TU Dortmund for funding. Conflict of interest The authors declare no conflict of interest.

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Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology.

Quorum sensing, the cell-to-cell communication system mediated by autoinducers, is responsible for regulation of virulence factors, infections, invasi...
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