Pantoea: insights into a highly versatile and diverse genus ...

FEMS Microbiology Reviews, fuv027, 39, 2015, 968–984

doi: 10.1093/femsre/fuv027Advance Access Publication Date: 24 June 2015Review Article

REVIEW ARTICLE

Pantoea: insights into a highly versatile and diversegenus within the EnterobacteriaceaeAlyssa M. Walterson and John Stavrinides∗

Department of Biology, University of Regina, 3737 Wascana Parkway, Regina, SK S4S 0A2, Canada∗Corresponding author: Department of Biology, University of Regina, 3737 Wascana Parkway, Regina, SK S4S 0A2, Canada. Tel: (306) 337-8478; Fax: (306)337-2410; E-mail: [email protected] sentence summary: This review synthesizes what is currently known about the diverse enterobacterial group, Pantoea, which not only exhibitsversatility in both host and non-host environments, but also shows biotechnological promise.Editor: Jan Roelof van der Meer

ABSTRACT

The bacterial genus Pantoea comprises many versatile species that have been isolated from a multitude of environments.Pantoea was delineated as a genus approximately 25 years ago, but since then, approximately 20 species have beenidentified having a diversity of characteristics. Isolates from water and soil have been harnessed for industrial purposesincluding bioremediation, and the degradation of herbicides and other toxic products. Other isolates possess nitrogenfixation and plant growth-promoting capabilities, which are currently being explored for agricultural applications. Someisolates are antibiotic producers, and have been developed into biocontrol agents for the management of plant diseases.Pantoea is also known to form host associations with a variety of hosts, including plants, insects and humans. Althoughoften thought of as a plant pathogen, recent evidence suggests that Pantoea is being frequently isolated from thenosocomial environment, with considerable debate as to its role in human disease. This review will explore this highlyversatile group and its capabilities, its known associations, and the underlying genetic and genomic determinants thatdrive its diversity and adaptability.

Keywords: Pantoea; enterobacterial plant pathogen; nitrogen fixation; opportunistic pathogen; soil; symbiont; mutualism;epiphyte; antibiotic production; human pathogen; bioremediation; biocontrol; Enterobacter agglomerans; Erwinia herbicola

INTRODUCTION

The genus Pantoea is a diverse group of yellow-pigmented, rod-shaped Gram-negative bacteria in the Enterobacteriaceae. Someof the first members were recognized as plant pathogens caus-ing galls, wilting, soft rot and necrosis in a variety of agricul-turally relevant plants, but since then, Pantoea strains have beenfrequently isolated from many aquatic and terrestrial environ-ments, as well as in association with insects, animals and hu-mans (Muraschi, Friend and Bolles 1965; Ewing and Fife 1972;Brady et al. 2008; Volksch et al. 2009; Nadarasah and Stavrinides2014). Some Pantoea isolates produce antimicrobials, and havebeen developed into commercial biocontrol products, such asBlightBan C9-1 and Bloomtime Biological, to help control fire

blight of apple and pear trees (Johnson et al. 1993, 2000; Johnsonand Stockwell 1998), while others have bioremediation poten-tial, with the capacity to degrade herbicides without the gen-eration of toxic by-products (Pileggi et al. 2012). As well, someisolates have been harnessed as immunopotentiators for the de-velopment of supportive drugs for melanoma, infections, aller-gies and the reversal of immunosuppression (Yoshida et al. 2009;Hebishima et al. 2011; Nakata, Inagawa and Soma 2011). Theubiquity, versatility and genetic tractability of Pantoea isolatesmakes it an ideal group for not only exploring niche-specificadaptation and opportunism, but also for the development ofcommercially relevant medical, agricultural and environmen-tal products. This review will examine the general biology of

Received: 25 August 2014; Accepted: 20 May 2015C© FEMS 2015. All rights reserved. For permissions, please e-mail: [email protected]

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Walterson and Stavrinides 969

Figure 1. Isolates of Pantoea have been isolated from a variety of soil andwater environments, aswell as in associationwith different hosts. Determinants for associatingwith various plants include the T3SS and T3SEs proteins (HsvG, HsvB and WtsE), as well as carotenoids and indole-3-acetic acid (IAA). Several determinants havealso been determined to be involved in the association of Pantoea with various insects, with almost no information on the factors that facilitate colonization of

mammalian hosts, including humans. Specific isolates and their natural products have shown promise for therapeutics, including cancer therapy and reversal ofimmunosuppression, while others have been explored for their bioremediation abilities, including degradation of organic materials and surfactant biosynthesis.Pantoea isolates continue to be evaluated for the biological control and management of plant pests, such as their ability to outcompete pathogens through competitiveexclusion and antibiotic production, and their ability to induce plant systemic resistance.

Pantoea, including its evolution, genomics and the specific ge-netic factors that contribute to its environmental versatility andhost-associating capabilities (Fig. 1).

CLASSIFICATION, SPECIES DIVERSITYAND PHYLOGENY

The early taxonomy of members of Pantoea is quite complex,with some of the first members of the group being classifiedas Bacillus agglomerans (Beijerinck 1888) and Enterobacter agglom-erans (Beijerinck 1888; Tindall 2014). Other names also associ-ated with members of this group included Bacterium herbicolaLohnis 1911, Pseudomonas herbicola (Geilinger 1921) de’Rossi 1927,Erwinia herbicola (Duggeli) Dye 1964 and E. milletiae (Kawakamiand Yoshida 1920) Magrou 1937, which were later established assynonymous by Ewing and Fife (1972) (Tindall 2014). Later, Beji(1988) and Gavini et al. (1989) recognized E. herbicola, E. milletiaeand En. agglomerans as also being synonymous, leading to thetransfer of these three groups to the proposed name, Pantoea ag-glomerans (Beijerinck 1888; Gavini et al. 1989), which served as the

nomenclatural type for the establishment of the genus, Pantoea(Ewing and Fife 1972; Beijerinck 1888; Gavini et al. 1989; Tindall2014).

With the delineation of the genus, the identification of newPantoea species has expanded substantially over the last severalyears. Pantoea is closely related to Tatumella and Erwinia (Bradyet al. 2010a,b), the three forming a monophyletic group nestedwithin the other enterobacterial genera, Escherichia, Salmonella,Citrobacter, Enterobacter, Klebsiella and Cronobacter (Fig. 2). Thebasal lineage to this monophyletic group contains a secondgroup that contains many enterobacterial plant pathogenicgroups, including Dickeya, Pectobacterium and Brenneria, alongwith the endosymbiont Sodalis (Fig. 2) (Stavrinides 2009). Pantoeais currently composed of 20 recognized species that are pheno-typically similar, and which were proposed to comprise a totalof 13 hybridization groups (Brady et al. 2008, 2009a,b, 2011, 2012;Popp et al. 2010). Pantoea type strains that define each respectivespecies group have been isolated from a number of sources, al-though mostly from plants (Table 1). A rooted phylogenetic treeof Pantoea type strains constructed using gyrB, rpoB and 16S rRNA

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Figure 2. Cladogram obtained from the Pathosystems Resource Integration Cen-

ter (Wattam et al. 2014), which was constructed using shared protein homologsderived from whole genomes of entire species groups within each genus in theEnterobacteriaceae. The relative position of Pantoea is indicated with a box. As ge-nomic information for Tatumella (sister taxon to Pantoea) has not yet been in-

corporated into the Pathosystems Resource Integration Center, it is not shown.Pseudomonas (Pseudomonadaceae) was used as the root.

shows the relationships between the established species groups(Fig. 3). Species like P. deleyi, P. anthophila, P. allii, P. cypripedii, P.wallisi, P. rodasii and P. rwandensis have been isolated from onlyplant sources, P. conspicua, P. brenneri, P. septica and P. eucrina from

only clinical sources and P. gavinae from only outdoor environ-mental sources. Isolates of P. calida, P. dispersa and P. gavinaewereidentified from the natural environment or processed products(Table 1). Previously, several other species had been proposed,including P. citrea, P. punctata and P. terrea (Kageyama et al. 1992);however, these were later reclassified into the genus Tatumellausingmultilocus sequence analysis (MLSA)methods (Brady et al.2010a,b).

ADVANCES IN OUR UNDERSTANDING OFPLANT-ASSOCIATED ISOLATES

Most of the early research on Pantoea focused on its parasiticassociation with plant hosts, including maize, cotton, melonand onion (Table 2) (Gitaitis and Gay 1997; Walcott et al. 2002;Medrano and Bell 2007; Kido et al. 2008; Brady et al. 2011).Plant diseases caused by phytopathogenic isolates are diverse(Table 2), and in some cases are shown to be facilitated by a suiteof pathogenicity factors that include the type III secretion sys-tem (T3SS), quorum-sensing systems and exopolysaccharides(EPS) (Roper 2011). The T3SS is responsible for the transport ofvirulence factors, or effector proteins, into host cells, resultingin the subversion of host defenses (Galan and Collmer 1999).For P. stewartii subsp. stewartii, the causative agent of Stewart’swilt disease in corn, the interaction with the host plant is medi-ated by a T3SS, PSI-1 (Correa et al. 2010, 2012). PSI-1 is a 24 kbgenomic island, similar to the Hrc-Hrp1 family of T3SSs thatis also found in P. agglomerans pv. gypsophilae (Frederick et al.2001; Coplin et al. 2002). Regulation of the PSI-1 T3SS involvesthe HrpX/HrpY two-component regulatory system (Merighi et al.2003, 2006). HrpY acts downstream in the activation of hrpS,which subsequently regulates hrpL in response to environmentalstimuli. HrpL, an alternate sigma factor, is then involved in theregulation and expression of effector genes (Merighi, Majerczakand Coplin 2005). HrpX, the other component in this regulatorysystem, is responsible for the expression of hrp genes and is ac-tivated under nutrient-limited conditions (Merighi et al. 2006).

Table 1. Pantoea type strains and source of isolation.

Species Type strain Origin Reference

P. agglomerans LMG 1286 Human, knee laceration Gavini et al. (1989)P. allii LMG 24248 Onion seed Brady et al. (2011)P. ananatis LMG 2665 Pineapple Mergaert, Verdonck and Kersters (1993)P. anthophila LMG 2558 Garden balsam Brady et al. (2009a,b)P. beijingensis LMG 27529 King trumpet mushroom Liu et al. (2013)P. brenneri LMG 5343 Human, urethra Brady et al. (2010a,b)P. calida LMG 25383 Powdered infant formula Popp et al. (2010)P. conspicua LMG 24534 Human, blood Brady et al. (2010a,b)P. cypripedii LMG 2657 Orchid Brady et al. (2010a,b)P. deleyi LMG 24200 Eucalyptus Brady et al. (2009a,b)P. dispersa LMG 2603 Soil Gavini et al. (1989)P. eucalyptii LMG 24197 Eucalyptus Brady et al. (2009a,b)P. eucrina LMG 2781 Human, trachea Brady et al. (2010a,b)P. gavinae LMG 25382 Powdered infant formula Popp et al. (2010)P. rodasii LMG 26273 Eucalyptus Brady et al. (2012)P. rwandensis LMG 26275 Eucalyptus Brady et al. (2012)P. septica LMG 5345 Human, stool Brady et al. (2010a,b)P. stewartii subsp. indologenes LMG 2632 Foxtail millet Mergaert, Verdonck and Kersters (1993)P. stewartii subsp. stewartii LMG 2715 Maize Mergaert, Verdonck and Kersters (1993)P. vagans LMG 24199 Eucalyptus Brady et al. (2009a,b)P. wallisii LMG 26277 Eucalyptus Brady et al. (2012)

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Figure 3.Neighbor-joining phylogeny of Pantoea type strains, based on a concate-nated dataset composed of partial rpoB, gyrB, atpD and 16S rRNA genes using

maximum composite likelihood. Nodes show the result of 1000 bootstrap repli-cates, with values >50% being shown. Symbols adjacent to each representativetype strain indicate whether strains within that species group have been iso-lated from clinical settings (red circle), from plant hosts either as an epiphyte or

a pathogen (green square), or from the natural environment (purple triangle).

Activation of the T3SS results in the injection of type III secretedeffectors (T3SEs) into the host cell, which function to facilitatehost-specific interactions between the bacteriumand host. HsvBand HsvG are T3SEs carried by P. agglomerans pv. betae and P. ag-glomerans pv. gypsophilae, respectively, and have been shown toplay an important role in host-specific colonization (Nissan et al.2006; Weinthal et al. 2011; Kirzinger and Stavrinides 2012). Theintroduction of HsvB into beet and HsvG into gypsophila influ-ences plant transcription and leads to gall formation. When theT3SEswere introduced into the other host (HsvB in gypsophila orHsvG into beet), then no galls would form, suggesting that hostspecificity is determined at the gene level (Nissan et al. 2006).

Quorum sensing is a process whereby bacteria monitor theirpopulation density through the use of small diffusible signalmolecules (Minogue et al. 2005; Koutsoudis et al. 2006), and canalso be involved in regulating gene systems for pathogenesis andhost interactions (Koutsoudis et al. 2006). For P. stewartii subsp.stewartii, quorum sensing influences adhesion, motility and dis-persion, as well as EPS production, and plays a major role in thedevelopment of Stewart’s wilt disease of corn (von Bodman, Ma-jerczak and Coplin 1998; Koutsoudis et al. 2006). Pantoea stewartiicolonizes the xylem of the plant where it multiples and pro-duces EPS, thereby blocking the flow of water and causing theplant to wilt. The production of the EPS is regulated through theEsaI/EsaR quorum-sensing system, which governs the cps genecluster that is responsible for EPS biosynthesis in a cell-density-dependent manner (Koutsoudis et al. 2006). EsaR is thought toact through the repression of the rcsA gene, which in turn acts asa coactivator for RcsA/RcaB-mediated transcriptional activationof the cps gene cluster (Minogue et al. 2002, 2005). EPS not onlyaids in the development of Stewart’s wilt disease symptoms, butis thought to also provide the invading bacteria with the neces-sary protection from plant host defenses (Wehland et al. 1999).The presence of the cps gene cluster is an important geneticcomponent in the overall pathogenicity of P. stewartii, along withthe T3SE, WtsE/AvrE, which results in water soaking, and subse-quent cell death in host plants (Ham et al. 2008).

Epiphytic populations of Pantoea have been identified onmany plants, as well as on vegetables, fruits and grains, sug-gesting they possess specific adaptations that facilitate colo-nization of the phyllosphere (Table 2) (Brandl and Lindow 1998;Beattie and Lindow 1999; Venturini, Oria and Blanco 2002; Lin-dow and Brandl 2003; Oie et al. 2008; Nadarasah and Stavrinides2014). For some isolates, the ability to compete and surviveepiphytically is facilitated by the production of indole-3-aceticacid, which has been shown to contribute to the overall nu-trient leakage of the plant leaves, and overall survival (Brandl,Clark and Lindow 1996; Brandl and Lindow 1998). Likewise, theproduction of carotenoids responsible for the bright yellow pig-ment appears to play a major role in resistance to ultraviolet(UV) radiation, which allows for successful epiphytic coloniza-tion (Mohammadi, Burbank and Roper 2012). Carotenoids, whichare often localized to the hydrophobic regions of themembrane,are able to protect the cell from harmful UV wavelengths (320–400 nm), as well as harmful reactive oxygen species that areactivated in the presence of UV during crucial growing phases(Mohammadi, Burbank and Roper 2012). Mutants that lackedpigmentation had an overall decreased survivorship over wildtype in the presence of H2O2 on nutrient-rich media (Moham-madi, Burbank and Roper 2012).

INSECT ASSOCIATIONS

Muchof the research surrounding the association of Pantoeawithinsects has stemmed from the specific adaptations of P. stew-artii subsp. stewartiiDC283 (DC283) to its flea beetle vector (Roper2011). The bacteria are carried in the insect gut, which are de-posited on the surface of sweet corn via the insect frass (Eskerand Nutter 2003; Menclas et al. 2006; Roper 2011). The bacteriagain entry into the plant via wounds created by the feeding bee-tles, which results in the colonization of either the apoplast orthe xylem vasculature, the production of EPS and the develop-ment of the characteristic wilt commonly attributed to P. stew-artii (Leigh andCoplin 1992). Persistencewithin the corn flea bee-tle gut by DC283 is facilitated by an animal-specific T3SS, PSI-2,which allows for successful colonization of the corn flea beetle,

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Table 2. Epiphytic and parasitic colonization of plants by strains of Pantoea.

Species Epiphyte Pathogen Disease/symptoms

P. agglomerans Cabbage1, leek1, spinach1, tomato1, kiwi1,persimmon1, wheat1, green bean2, oat seed2, soybean2, onion2, baby’s breath2, raspberry bush2,rose bush2, Virginia creeper2, cherries2

Pea9, sweet corn10, sweetpotato11, sugarcane12,bamboo13, wheat14.

Various

Cotton10 Seed and ball rot35

Eucalyptus15 Bacterial blight and diebackGypsophila paniculata16 GallRice17 Red stripeBeach pea18 Black spot necrosisChinese taro19 Bacterial spotBeet20 Tumors

P. allii Onion21 Centre rotP. ananatis Rice2, pineapple3 Bamboo13, switchgrass22 Various

Rice23 Stem necrosisNetted melon24 Fruit rotOnion Centre rot36, bulb decay37

Sudangrass25 Leaf blotchEucalyptus26 Bacterial blight and diebackCorn27 Leaf spot diseaseAgave28 Red leaf ring

P. anthophila Balsam2, 4

P. beijingensis Pleurotus eyringii5

P. cypripedii Orchid6

P. deleyi Eucalyptus4

P. dispersa Sorghum2 Grape29

Sugarcane12

P. eucalyptii Thistle2

Eucalyptus4

P. rodasii Eucalyptus7

P. rwandensis Eucalyptus7

P. stewartii Steria italia3 Cotton30 Seed rotSudangrass25 Leaf blotchEucalyptus26 Bacterial blight and diebackCorn3, 31 Stewart’s wilt

P. vagans Eucalyptus4

P. wallisii Eucalyptus7

Pantoea sp. Plum8 Sugarcane32

Deepwater rice33, 34

1Oie et al. (2008), 2Nadarasah and Stavrinides (2014), 3Mergaert, Verdonck and Kersters (1993), 4Brady et al. (2009a,b), 5Liu et al. (2013), 6Brady et al. (2010a,b), 7Brady et al.

(2012), 8Janisiewicz et al. (2013), 9Elvira-Recuenco and van Vuurde (2000), 10McInroy and Kloepper (1995), 11Asis and Adachi (2004), 12Magnani et al. (2013), 13Nadha et al.

(2012), 14Stets et al. (2013), 15Brady et al. (2009a,b), 16Cooksey (1986), 17Guanlin (2001), 18Khetmalas et al. (1996), 19Romeiro et al. (2007), 20Burr et al. (1991), 21Brady et al.

(2011), 22Gagne-Bourgue et al. (2013), 23Cother et al. (2004), 24Kido et al. (2008), 25Azad, Holmes and Cooksey (2000), 26Coutinho et al. (2002), 27Perez-y-Terron et al. (2009),28Fucikovsky and Aranda (2006), 29Nisiotou et al. (2011), 30Bell et al. (2004), 31Roper (2011), 32Loiret et al. (2004), 33Verma et al. (2004), 34Laskar, Nevita and Sharma (2012),35Medrano and Bell (2007), 36Walcott et al. (2002), 37Gitaitis and Gay (1997).

as well as the subsequent transmission of P. stewartii to cornplants (Correa et al. 2012). The PSI-2 system belongs to the Inv-Mxi-Spa group of T3SSs that aid in animal cell invasion by bacte-ria (Correa et al. 2012). An effector gene, ospC1, is thought to playa role in post-invasion pathogenesis of the flea beetle by DC283(Correa et al. 2012). This same strain however, is pathogenic to-wards the pea aphid, suggesting possible opportunistic interac-tionswith other insect hosts in the environment (Stavrinides, Noand Ochman 2010). DC283 carries the ucp1 gene, whose productappears to enable bacterial aggregation and adhesion, allowingDC283 to colonize the aphid hindgut and crop (Stavrinides, Noand Ochman 2010). Disruption of this gene in wild-type DC283prevents colonization of the aphid, suggesting that ucp1 is re-sponsible for this interaction. The role of ucp1 in the colonizationof the flea beetle, if any, remains to be determined.

In addition to the flea beetle, a wide variety of insect speciesappear to have associations with different Pantoea isolates(Table 3). Several of these associations have been described asmutualistic, wherein the bacteria are found to inhabit the in-sect intercellularly, and in some cases intracellularly within spe-cialized cells of the symbiont host (Vorwerk, Blaich and Forneck2007). In suchmutualisms, the insect host has been suggested toprovide the bacteria with nutrients and habitat, and possibly adirect means of dispersal (Sood and Nath 2002), while the insectmay benefit frombacteria-mediated hydrolysis of proteins (Soodand Nath 2002), antagonism of pathogens (Vorwerk, Blaich andForneck 2007), breakdown of toxic substances (Sood and Nath2002), nitrogen fixation (Maccollom et al. 2009), nutrition and di-gestion (Maccollom et al. 2009). The blueberry maggot fly, for ex-ample, has been reported to form amutualistic association with

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Table 3. Colonization of insect, animals and humans by strains of Pantoea.

Species Insects Animals HumansAssociated humandisease/condition

P. agglom-erans

Pea aphid1, wood-boringbeetle2, locust3, fruit fly4, 5,honey bee6, tobacco thrip7,grape Phylloxera8, caterpillar9,blueberry maggot fly10, pecanPhylloxera11, grass grub9,Phlebotomus papatasi12, Asianlonghorned beetle13, Plagioderaversicolora14

Horse24, brown trout25, 26,chicken27, rainbow trout26,mangrove crab28, dolphinfish29, chinook salmon30,slug9, giant panda31

Wounds9, fractures36, surfaceswab37, sputum37, urine9, earswab9, oropharynx swab9,knee laceration38

Septic arthritis41,osteomyelitis42, 43

bacteremia44, 45, 46,septicemia47,nosocomialinfection48, 49,peritonitis50, 51, 52,sepsis53, 54, septicmonoarthritis55,liver abscess56, 57,

periodontaldisease58,

pneumonia59, 60,respiratorydistress61, 62, 63, 64,acute hip prosthesisjoint infection65

P. ananatis Tobacco thrip7, cotton Corneal infiltration66

fleahopper15, Lygus hesperus16 Bacteremia67

P. brenneri Wounds9, sputum39, groinswab9, abscesses9, urethralswab9, 39

P. calida Urine9, dialysate9

P.conspicua

Wounds9, blood9, 40

P. dispersa Blood9 Nosocomialinfection68

P. eucrina Blood9, spinal fluid39, cysts39,trachea swab39

P. septica Blood39, skin swab39,sputum9, finger swab9,urine9, stool39

P. stewartii Mosquito17, corn flea beetle18,pea aphid19

Goose9

Pantoea Pine engraver20, leaf-cutter Ostrich32, deer33, dunnock34, Nosocomialsp. ant21, stink bug22, cow35 infection61 Sepsis69

Phlebotomine sand fly23 Dacryocystitis70

1Harada, Oyaizu and Ishikawa (1996), 2Delalibera, Handelsman and Raffa (2005), 3Dillon and Charnley (1995), 4Sood and Nath (2002), 5Lauzon et al. (2009), 6Loncaric et al.(2009), 7Wells, Gitaitis and Sanders (2002), 8Vorwerk et al. (2007), 9Nadarasah and Stavrinides (2014), 10Maccollom et al. (2009), 11Medina, Nachappa and Tamborindeguy(2011), 12Maleki-Ravasan et al. (2014), 13Podgwaite et al. (2013), 14Demirci et al. (2013), 15Bell et al. (2007), 16Cooper, Nicholson and Puterka (2013), 17Terenius et al. (2012),18Esker and Nutter (2003), 19Stavrinides, No and Ochman (2010), 20Delalibera et al. (2007), 21Pinto-Tomas et al. (2009), 22Prado and Almeida (2009), 23Akhoundi et al. (2012),24Hong et al. (1993), 25Loch and Faisal (2007), 26Carbajal-Gonzalez et al. (2012), 27Volksch et al. (2009), 28Vieria et al. (2004), 29Hansen, Raa and Olafsen (1990), 30Sauteret al. (1987), 31Li et al. (2012), 32Cabassi et al. (2004), 33Muraschi, Friend and Bolles (1965), 34Kiskova et al. (2012), 35Verdier-Metz et al. (2012), 36Slotnick and Tulman (1967),37Cruz, Cazacu and Allen (2007), 38Gavini et al. (1989), 39Brady et al. (2010a,b), 40Brady et al. (2009a,b), 41Flatauer and Khan (1978), 42Vincent and Szabo (1988), 43Labianca

et al. (2013), 44Aly et al. (2008), 45Christakis et al. (2007), 46Lalas and Erichsen (2010), 47Bergman, Arends and Scholvinck (2007), 48Bicudo et al. (2007), 49Boszczowski et al.(2012), 50Borras et al. (2009), 51Ferrantino, Navaneethan and Sloand (2008), 52Lim et al. (2006), 53Cicchetti et al. (2006), 54Kratz et al. (2003), 55Ulloa-Gutierrez, Moya andAvila-Aguero (2004), 56Rodrigues et al. (2009), 57Fullerton, Lwin and Lal (2007), 58Goncalves et al. (2007), 59Shubov, Jagannathan and Chin-Hong (2011), 60Kursun et al.

(2012), 61Van Rostenberghe et al. (2006), 62Skorska et al. (2003), 63Milanowski (1994), 64Golec et al. (2004), 65Hischebeth et al. (2013), 66Manhoran et al. (2012), 67De Baere

et al. (2004), 68Schmid et al. (2003), 69Habsah et al. (2005), 70Zuberbuhler, Carifi and Leatherbarrow (2012).

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P. agglomerans, whereby the bacterium carries out essential ni-trogen cycling processes in the host gut, while the fly providesnutrition and a suitable habitat (Maccollom et al. 2009). Blueberrymaggot flies are naturally attracted to the degradation productsof uric acid, as well as the production of other volatile chemi-cals (Maccollom et al. 2009). Strains producing uricase are ableto break down uric acid, thus attracting the flies to their foodsource and facilitating the association between the symbionts(Robacker and Lauzon 2002; Maccollom et al. 2009).

Several Pantoea–insect associations identified appear to becommensalistic. The leaf-cutter ant, which cultivates its ownfungus gardens for food is an important player in nutrient cy-cling in forest environments (Wirth et al. 2003; Pinto-Tomaset al. 2009). Pantoea sp. At-9b was consistently isolated as oneof the nitrogen-fixing bacterial groups from the fungus gar-dens, with some isolates carrying a gene cluster that codes forthe molybdenum–iron nitrogen fixation pathway (Pinto-Tomaset al. 2009). The nitrogen fixation provided by Pantoea sp. At-9b and other microbes in these fungus gardens is thought toallow the leaf-cutter ants to use a wider variety of leaf mate-rial that has lower nitrogen concentrations (Pinto-Tomas et al.2009). Whether these bacteria are carried by and inoculated bythe ants, or whether they are naturally present in the soil is cur-rently unknown.

DEADLY PATHOGEN, HARMLESS COMMENSALOR VERSATILE OPPORTUNIST?

There is presently considerable debate as to the animalpathogenic capabilities of different Pantoea species groups.Strains of P. septica, P. calida, P. dispersa, P. ananatis, P. agglom-erans and P. eucalyptii have been isolated routinely from hu-man wounds, fractures, blood and other fluids, skin and sur-face swabs, stool, cysts and abscesses, as well as from swabs ofthe urethra, trachea and oropharynx (Table 3) (Slotnick and Tul-man 1967; Cruz et al. 2007; Coutinho and Venter 2009; Brady et al.2010a,b; Nadarasah and Stavrinides 2014). Pantoea strains havebeen identified from both immunocompetent and immunocom-promised patients, with patient age ranging from premature in-fants to seniors (Flatauer and Khan 1978; Vincent and Szabo1988; Kratz et al. 2003; Schmid et al. 2003; De Baere et al. 2004;Christakis et al. 2007; Aly et al. 2008). Introduction of the bacteriainto or onto the patient has been proposed to be through con-tamination ofmedical instruments and parenteral (intravenous)nutrition, inhalation of organic dust, wounds exposed to organicmaterial or perinatal in nature (Milanowski 1994; De Champset al. 2000; Skorska et al. 2003; Cicchetti et al. 2006; Van Ros-tenberghe et al. 2006; Bicudo et al. 2007; Cruz et al. 2007; Hsiehet al. 2007; Ferrantino, Navaneethan and Sloand 2008; Lee, Chungand Park 2010). A wide range of afflictions have been ascribed toPantoea, including septic arthritis, osteomyelitis, bacteremia andsepticemia, and peritonitis, among many others, although di-rect causation for most of these has not been demonstrated (Ta-ble 3) (Flatauer and Khan 1978; Vincent and Szabo 1988; De Baereet al. 2004; Lim et al. 2006; Bergman, Arends and Scholvinck 2007;Christakis et al. 2007; Aly et al. 2008; Ferrantino, Navaneethanand Sloand 2008; Borras et al. 2009; Lalas and Erichsen 2010; Labi-anca et al. 2013). Several neonatal outbreaks, however, resultedinmultiple deaths from septicemic shock and respiratory failure(Van Rostenberghe et al. 2006; Bergman, Arends and Scholvinck2007). Some work, however, has suggested that these and manyother clinical isolates that have been labeled as a strain of Pan-

toea are, in fact, misidentified (Rezzonico, Smits and Duffy 2012).One study demonstrated that clinical and animal isolates re-ported as members of Pantoea (and most frequently as P. agglom-erans) actually belong to other Pantoea species groups, and evenother genera, like Enterobacter (Rezzonico et al. 2009). In caseswhere clinical isolates are confirmed to be Pantoea, they belongto multiple species groups, including P. septica, P. calida, P. bren-neri, P. eucalyptii and P. agglomerans (Nadarasah and Stavrinides2014).

To try to understand the pathogenic potential of Pantoea iso-lates, and whether there is evidence for the evolution of hostassociation and/or host specialization among lineages, severalMLSA studies have been conducted using collections of vali-dated clinical and environmental Pantoea isolates to evaluatethe extent to which clinical and environmental isolates cluster(Brady et al. 2008, 2009a,b, 2010a,b; Deletoile et al. 2009; Rezzon-ico et al. 2009; Nadarasah and Stavrinides 2014). The separatephylogenetic clustering of clinical and environmental isolates—grouping into pathogenic and non-pathogenic groups—is con-sidered strongly supportive of lineage-specific host adaptation,as seen with other enterics like Escherichia coli (Georgiadesand Raoult 2011). In all phylogenetic studies carried out forPantoea, environmental and clinical isolates of many speciesgroups including P. agglomerans, P. ananatis and P. eucalyptii donot form distinctive clusters within each respective speciesgroup, but rather are intermingled (Brady et al. 2008, 2009a,b,2010a,b; Deletoile et al. 2009; Rezzonico et al. 2009; Nadarasahand Stavrinides 2014). This phylogenetic structure is generallysuggestive of isolates having an unknown capacity for host as-sociation, with clinical isolates possibly having the potential tocolonize plant hosts, and environmental isolates having the po-tential to colonize human hosts (Nadarasah and Stavrinides2014). In addition, a split decomposition analysis of P. agglom-erans has revealed substantive recombination between isolates(Deletoile et al. 2009), demonstrating a capacity for transfer ofgenetic determinants between individual isolates with differentcapabilities.

The evaluation of virulence potential of both plant and clin-ical Pantoea isolates has also been carried out using functionalhost assays. One study, which examined the virulence potentialof multiple species of Pantoea from environmental and clinicalsources using quantitative growth assays in maize, onion andfruit flies, showed that clinical isolates were able to grow in bothplant hosts comparably to environmental isolates (Nadarasahand Stavrinides 2014). There were no apparent growth or hostcolonization patterns that were unique to clinical isolates, andhost growth could not be predicted by phylogeny or source ofisolation (Nadarasah and Stavrinides 2014). A separate studyevaluated five clinical and five plant-associated P. agglomeransstrains quantitatively in both soybean and embryonated heneggs (Volksch et al. 2009). Both clinical and plant strains wereable to establish epiphytically on soybean plants, and there wasno difference in virulence between clinical and plant isolates inthe embryonated egg, suggesting that all P. agglomerans isolatesmight possess equal virulence potential (Volksch et al. 2009).Both of these studies indicate that the host-colonizing capabili-ties of Pantoea isolates remain unpredictable, with an unknownplant or animal host range/host-associating capacity for mostisolates. Notably, Pantoea strains are also found to be associatedwith terrestrial and aquatic animals, including birds, fish, inver-tebrates, bears and ruminants, which could be suggestive of alife history that involves animal hosts (Table 4) (Muraschi, Friendand Bolles 1965; Sauter et al. 1987; Hansen, Raa andOlafsen 1990;

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Table 4. Pantoea isolations from soil and water environments.

Species Soil Source Water Source Location

P. agglomerans Mangrove sludge1, 2 Aquifer Bangladesh10

Pond sediment3 Thermal spring Spain11

Iron-rich soil4 Drinking water South Africa12

High salt and pH soil5 River Chile13

P. ananatis Aquatic environment adjacent to agriculture Brazil14

P. anthophila Drinking water India15

P. dispersa Sub-alpine soil6, soil7

Pantoea sp. Olive mill waste8

Kerosene-rich soil9

1Liu et al. (2012), 2Yeung, Lee and Woodard (1998), 3Francis, Obraztsova and Tebo (2000), 4Sulbaran et al. (2009), 5Son et al. (2006), 6Selvakumar et al. (2008), 7Gavini et al.(1989), 8Pepi et al. (2010), 9Vasileva-Tonkova and Gesheva (2007), 10Sultana et al. (2011), 11Mosso et al. (1994), 12September et al. (2007), 13Escalante et al. (2009), 14Pileggiet al. (2012), 15Pindi, Yadav and Shanker (2013).

Cabassi et al. 2004; Vieria et al. 2004; Loch and Faisal 2007; Volkschet al. 2009; Carbajal-Gonzalez et al. 2012; Kiskova et al. 2012; Liet al. 2012; Verdier-Metz et al. 2012; Nadarasah and Stavrinides2014).

GENETICS AND GENOMICS

There are still considerable gaps in our knowledge of the spe-cific genetic determinants that allow Pantoea isolates to be a suc-cessful colonizer of both host and non-host environments. ForP. stewartii subsp. stewartii and its association with sweet corn,the T3SS (PSI-1) and the EPS, stewartan, appear to be the mainvirulence factors (Roper 2011). Association of P. stewartii subsp.stewartiiwith its flea beetle vector is facilitated by the T3SS, PSI-2. For P. agglomerans phytopathogenicity, the T3SS along withother virulence factors such as T3SEs are required, which arecarried on a plasmid (pPATH) that was suggested to have beenacquired horizontally fairly recently (Clark et al. 1993; Nizanet al. 1997; Valinsky et al. 1998; Ezra et al. 2004; Weinthal et al.2007). Aside from this and a few other select strains, the de-terminants used by most other Pantoea species for establish-ing in both host and non-host environments remains largelyunderexplored.

The availability of sequenced Pantoea genomes has allowedfor the discovery and comparison of genetic factors that maycontribute to the ability of certain isolates to thrive in dif-ferent environments. The genomes of several isolates of Pan-toea, such as P. agglomerans, P. stewartii, P. vagans and P. ana-natis, have been published, revealing genome sizes from 4.5 to6.3 MB and G+C contents of 52–55% (Smits et al. 2010, 2011;Choi et al. 2012; De Maayer et al. 2012b; Hong et al. 2012; Kimet al. 2012; Matsuzawa et al. 2012; Medrano and Bell 2012;Remus-Emsermann et al. 2013; Smith, Kirzinger and Stavrinides2013; Walterson, Smith and Stavrinides 2014). Although therehas been no broad-scale systematic comparative or evolution-ary genomic analysis of Pantoea as of yet, some common ge-nomic features identified inmore specific analyses include acyl-homoserine lactones and other quorum-sensing genes (Smitset al. 2010; Hong et al. 2012), plant growth-promoting genes (Kimet al. 2012), DNA repair genes (Remus-Emsermann et al. 2013),pathogenicity factors (De Maayer et al. 2010, 2012a), as well astype IV and VI secretion systems (Kim et al. 2012; Medrano andBell 2012).

A recent comparative genomic analysis of the type VI se-cretion system (T6SS) was conducted using sequenced Pantoeaand Erwinia genomes, which showed that one T6SS variant was

prevalent in Pantoea isolates from diverse environments (DeMaayer et al. 2011). One locus in particular, the T6SS-1 locus, con-tains two highly conserved core regions that alternate with vari-able regions containing hcp and vgrG, which code for secretedeffector proteins (De Maayer et al. 2011). The hcp and vgrG is-lands contain domains that are conserved across Pantoea strains,and show homology to genes with known roles in antibiosis,fungal cell wall degradation, and animal and plant pathogen-esis (De Maayer et al. 2011). However, the presence of these do-mains in isolates from diverse environments suggests that theremay be an innate capability for genetic versatility and adapt-ability. This adaptability is also reflected in the plasmids of Pan-toea. A comparative genomic study of at least 20 isolates led tothe identification of the Large Pantoea Plasmid family (LPP-1),which ranges from 280 to 789 kb, andwas found to be distributedamong 20 Pantoea isolates representing seven different species,including P. agglomerans, P. vagans, P. eucalyptii, P. anthophila, P.stewartii, P. ananatis and P. cypripedii (De Maayer et al. 2012a).Plasmid-encoded loci are linked to metabolism and transporta-tion of various sugars, carbohydrates, amino acids and organicacids, as well as the assimilation of iron and nitrogen, antibi-otic and heavy metal resistance, host colonization, pathogene-sis and antibiosis (De Maayer et al. 2012a). This illustrates theplasticity of this plasmid family, which may contribute to thediversity of capabilities among the isolates of different speciesgroups.

There are still considerable gaps in our understanding ofthe nature of those determinants that provide Pantoea withenvironmental versatility, and how these determinants maybe regulated by each respective environment. This avenueof research has the potential to advance our understand-ing of host association and the factors that may enable op-portunism or niche expansion in particular species groups.Likewise, genome-level analyses of Pantoea can provide addi-tional information on the biology and evolution of this group,although these have been limited by the availability of fullysequenced genomes spanning the diversity of the genus. Ge-nomic comparisons, while mostly limited to small groups ofisolates, have yielded important insight into the nature of vir-ulence, resistance and metabolic determinants that confer keysurvival and host-association capabilities. The availability of ad-ditional genomes will enable larger comparative genomic anal-yses that can identify the specific evolutionary processes thatare responsible for species-level diversification. Such studieswould also allow for the assessment of the pathogenic po-tential of individual Pantoea isolates given the current use of

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some isolates as biocontrol, bioremediation and therapeuticagents.

PANTOEA IN BIOTECHNOLOGY

Many strains of Pantoea show striking environmental versatil-ity and adaptability, and possess a variety of biosynthetic andbiodegradative capabilities that can be harnessed for potentiallyuseful applications in agricultural, environmental and clinicalsettings.

Biocontrol

Plants are susceptible to colonization by a variety of phy-topathogenic bacteria and fungi, yet epiphytic colonization byPantoea has been shown to decrease the incidence of plant dis-ease (Johnson et al. 1993, 2000; Johnson and Stockwell 1998).Many Pantoea strains have been shown to be strong environmen-tal competitors that produce a variety of natural products withantibiotic activity, such as pantocins, herbicolins, microcins andphenazines (Wright and Beer 1996, 2002; Vanneste et al. 2000,2002; Vanneste, Yu and Reglinski 2002; Giddens, Feng and Ma-hanty 2002; Wright et al. 2006; Vanneste, Yu and Cornish 2008;Smits et al. 2010, 2011), as well as the more recent PNP-1 nat-ural product from P. ananatis BRT175 that has inhibitory activ-ity against E. amylovora, and which is likely similar to FVG, or4-formylaminooxyvinylglycine (Halgren et al. 2013; Trippe et al.2013; Walterson, Smith and Stavrinides 2014). Because of the di-versity of natural products they produce, along with their abilityto persist in the environment, some Pantoea strains have beendeveloped into commercial biocontrol products, such as Blight-Ban C9-1 and Bloomtime Biological, which utilize P. vagans C9-1 and P. agglomerans E325, respectively (Johnson and Stockwell1998; Pusey 2002). These biological control agents are used forfruits, vegetables and other crop plants to control many typesof Gram-negative and Gram-positive bacteria, pathogenic fungiin the Ascomycota and Basidiomycota, pathogenic oomycetesand parasitic nematodes (Table 5). Penicillium digitatum, for ex-ample, is a green mold that is responsible for post-harvest de-cay of citrus fruits (Poppe, Vanhoutte and Hofte 2003). Pantoeaagglomerans CPA-2 when applied during post-harvest has shownto be effective against Penicillium sp. under certain environmen-tal conditions (Canamas et al. 2008; Zamani et al. 2009). Whilethe exact mechanism for the control of Penicillium sp. is stillunclear, it may involve a combination of antifungals and an-tagonism through competitive colonization. Alternatively, Pan-toea may provide protection by inducing plant systemic resis-tance (Munif, Hallmann and Sikora 2001). The production ofcertain compounds, such as 1,2,3-benzothiadiazole carbothioicacid S-methyl ester or harpin, induces plant defenses, as shownthrough the production of β-1,3-glucanases or peroxides (H2O2)(Zhang et al. 1998; Vanneste et al. 2002). Pantoea-induced en-hancement of plant defenses has been used to protect tomatofrom the nematode, Meloidogyne incognita (Munif, Hallmann andSikora 2001), cucumber from the fungus, Colletotrichum orbiculare(Zhang et al. 1998),Arabidopsis from Pseudomonas syringae pv.ma-culicola (Zhang et al. 1998), and kiwifruit and tobacco from Scle-rotinia sclerotiorum (Vanneste et al. 2002). M. incognita is knownto produce root knots on tomato plants (Munif, Hallmann andSikora 2001). Pantoea agglomerans MK-29 was shown to inducesystemic resistance of the tomato plant when used as a soildrench, resulting in a decrease in penetration of the plant rootsby juvenile nematodes, and thereby preventing the developmentof root knots (Munif, Hallmann and Sikora 2001).

Bioremediation

Isolates of Pantoea have been identified in a wide variety of pris-tine and contaminated aquatic and terrestrial environments (Ta-ble 5). In the arsenic-contaminated waters of Bangladesh andChile, Pantoea isolates show arsenic resistance and/or degrada-tion capabilities (Escalante et al. 2009; Sultana et al. 2011). InBrazil, a P. ananatis isolate has shown the ability to break downthe herbicide, mesotrione (Pileggi et al. 2012). Since this environ-ment is adjacent to key agricultural sites, the degradation of her-bicides from agricultural run-off is one important strategy forprotecting aquatic species. Other isolates from a petrochemicalwastewater treatment plant showed the ability to absorb, accu-mulate and tolerate significant levels of copper, chromium andcadmium (Ozdemir et al. 2004). Since the presence of heavymet-als in aquatic environments has been shown to be toxic and car-cinogenic (Ruiz-Manriquez et al. 1998), the use of heavy metal-tolerant Pantoea isolates for the removal of these compoundsfrom wastewaters is of great interest to industry, and of partic-ular environmental significance (Ozdemir et al. 2004).

Pantoea soil isolates have been shown to possess capabil-ities that include metal reduction (Francis, Obraztsova andTebo 2000), solubilization and degradation of organic materi-als (Dastager, Deepa and Pandey 2009; Sulbaran et al. 2009), bio-surfactant production (Vasileva-Tonkova and Gesheva 2007; Ja-cobucci, Oriani and Durrant 2009), iron-based respiration (Wuet al. 2010) and solubilization of insoluble inorganics (Son et al.2006). Petroleum, or crude oil, often poses a significant envi-ronmental danger to marine life and coast-line terrestrial biota,such as those in the Antarctic, because of its ability to persistat toxic levels in the environment (Vasileva-Tonkova and Ge-sheva 2007). An antarctic strain, Pantoea sp. A-13, produces gly-colipid biosurfactants when using the petroleum hydrocarbons,kerosene and n-paraffin as its sole carbon and energy source(Vasileva-Tonkova and Gesheva 2007). These biosurfactants, inturn, result in the emulsification and subsequent biodegrada-tion of the harmful petroleum hydrocarbons (Vasileva-Tonkovaand Gesheva 2007). The use of naturally occurring isolates withthe ability to degrade toxic petroleum hydrocarbons into lessharmful compounds is a promising alternative to currently usedchemical surfactants (Vasileva-Tonkova and Gesheva 2007).

Biosensors and indicators

Some of the more phenotypically distinct isolates of Pantoeaare being explored for their potential as biosensors. One P. ag-glomerans isolate was found to produce a blue pigment in atemperature-dependent manner (Fujikawa and Akimoto 2011).Pigment production was determined to be cell density depen-dent, with cell densities of 106–108 being required for maximalpigment production; however, biosynthesis was also tempera-ture dependent, with bacteria acquiring the blue coloration attemperatures ≥10oC, and retaining their characteristic yellowcoloration at temperatures ≤10oC (Fujikawa and Akimoto 2011).Modeling of blue pigment production yielded a robust descrip-tion of its accumulation and biosynthesis, with the capacity tobe developed into a time-temperature indicator for use in mon-itoring of possible spoilage of food and clinical products (Fu-jikawa and Akimoto 2011).

Therapeutics

Although Pantoea is currently considered problematic in theclinical environment, products derived from Pantoea have been

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Table 5. Uses and potential uses of Pantoea strains for biocontrol and bioremediation.

Biocontrol Bioremediation

SpeciesPlant orcrop Pathogen/pest controlled Source Application

P. agglomerans Apple Botrytis cinerea1 Aquifer Arsenic resistance and/ordegradation23

Pear Botrytis cinerea1 Salt pond sediment Reduction of iron, manganese,chromium24

Penicillium expansum1 Iron-rich soil Solubilization of insolubleinorganic compounds25

Erwinia amylovora2 Crude oil contaminatedsoil

Biosurfactant production26

Lentil Botrytis cinerea3 Subterranean forestsediment

Reduction of iron27

Banana Botryodiplodia theobromae4 Soybean rhizosphere Solubilization of insolubleinorganic phosphates28

Colleotrichum musae4

Citrus fruit Penicillium digitatum5, 6, 7, 8

Penicillium italicum5, 6

Lemon Aspergillus flavus9

Potato Pectobacterium carotovorum ssp.atroseptica10

Radish Xanthomonas campestris11, 12

Cucumber Sclerotinia sclerotiorum9

Colletotrichum orbiculare3

Sugar beet Pythium sp.13

Safflower Pythium sp.13

Canola Pythium sp.13

Dry pea Pythium sp.13

Olive knot Pseudomonas savastanoi pv.savastanoi14

Centellaasiatica

Pseudomonas aeruginosa15

Tomato Meloidogyne incognita16

Arabidopsis Pseudomonas syringae pv. maculicola17

Kiwi Sclerotinia sclerotiorum18

Tobacco Sclerotinia sclerotiorum18

Soybean Pseudomonas syringae pv. glycinea19

P. ananatis Pome fruit Penicillium expansum20 Agricultural watersource

Degradation of mesotrione29

Pantoea sp. Potato Giberella pulicaris21 Wastewater treatmentsludge

Biosorption of copper,chromium, cadmium30

Lettuce Escherichia coli22 Ghat forest soil Biodegradation of phenol31

Spinach Escherichia coli22 Ornithogenic soil Biosurfactant production32

1Nunes et al. (2002), 2Pusey et al. (2011), 3Huang and Erickson (2002), 4Gunasinghe, Ikiriwatte and Karunaratne (2004), 5Canamas et al. (2008), 6Poppe, Vanhoutte and

Hofte (2003), 7Usall et al. (2001), 8Zamani et al. (2009), 9Kotan, Dikbas and Bostan (2009), 10Sturz and Matheson (1996), 11Han et al. (2000), 12Arsenijevic et al. (1998),13Bardin et al. (2003), 14Marchi et al. (2006), 15Rafat, Philip and Muniandy (2012), 16Munif et al. (2001), 17Zhang et al. (1998), 18Vanneste et al. (2002), 19Volksch, Ullrichand Fritsche (1993), 20Torres et al. (2005), 21Schisler and Slininger (1994), 22Johnston, Harrison and Morrow (2009), 23Sultana et al. (2011), 24Francis, Obraztsova and Tebo(2000), 25Sulbaran et al. (2009), 26Jacobucci et al. (2009), 27Wu et al. (2010), 28Son et al. (2006), 29Pileggi et al. (2012), 30Ozdemir et al. (2004), 31Dastager, Deepa and Pandey

(2009), 32Vasileva-Tonkova and Gesheva (2007).

developed into novel therapeutics. Recently, an immunopoten-tiator, IP-PA1, produced by P. agglomerans IG1 was shown to en-hance immune-related functions against bacterial and parasiticinfections in both mice and chickens (Kohchi et al. 2006) andenhance recovery from immunosuppression (Hebishima et al.2010a,b,c). IP-PA1 administered to mice with B16 melanoma, acancer of the skin, resulted in increased levels of tumor necro-sis factor-α, and prolonged survivorship significantly over micenot treated with the immunopotentiator (Hebishima et al. 2011).IP-PA1 has also been studied for use in macrophage activa-tion in the protection against infections, allergies and cancer,and the reversal of immunosuppression due to chemotherapy(Hebishima et al. 2010a,b,c, 2011), reflecting the potential ofPantoea-derived natural products as therapeutics.

CONCLUSIONS

Pantoea is a highly diverse group whose members are found inaquatic and terrestrial environments, and in association withplants, insects, humans and animals. While colonization by cer-tain Pantoea species is linked to diseases in plants, humans andanimals, some isolates formmutualistic associations or possessplant growth-promoting capabilities. Pantoea enhances insectfitness through the breakdown of toxic substances, and even fa-cilitate nitrogen fixation in plant roots under nitrogen-limitingconditions. In addition, the ability of this bacterial group to com-pete and survive in diverse environments has made many of itsmembers particularly attractive for both biocontrol and biore-mediation. Select strains of Pantoea have been developed into

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biocontrol agents, which prevent plant disease through the an-tagonism of pathogens, and in some cases, through the induc-tion of plant systemic defenses. Additionally, Pantoea has uniquebiodegradative capabilities, including metabolic pathways thatdegrade herbicides and other toxic compounds, providingopportunity for the development and commercialization ofuseful products; however, there is still much uncertainty sur-rounding the host-associating and pathogenic capabilities of in-dividual strains. The development of Panotea as bioagents mustbe considered carefully, given that there are no known pathogenbiomarkers available, and that clinical and environmental iso-lates are phylogenetically indistinguishable in all published phy-logenetic trees (Brady et al. 2008, 2009a,b, 2010a,b; Deletoile et al.2009; Rezzonico et al. 2009; Nadarasah and Stavrinides 2014). Ul-timately, there remains a need to identify those genetic deter-minants that enable niche-specific colonization, including anyfactors that may determine host-colonizing capacity and hostspecificity. Determining the nature of these genetic factors re-mains a promising research direction, andwill undoubtedly helpto unravel the full capabilities of this versatile, broad-niche bac-terial group.

FUNDING

This work was supported by Discovery Grants from the Natu-ral Sciences and Engineering Council (#386654), and a CanadaFoundation for Innovation LOF (#28591).

Conflict of interest. None declared.

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