Pseudomonas Lipopeptides in the Biocontrol of Plant Pathogens: Comparison
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The Pseudomonas genus is ubiquitous and comprises species which are well known phytopathogens, such as P. syringae, or opportunistic human pathogens, such as P. aeruginosa, but also host members associated with water, soil and plant surfaces. Pseudomonas spp. are well adapted to growing in the rhizosphere and are well suited for biocontrol and growth promotion. Pseudomonas lipopeptides (Ps-LPs) play crucial roles in bacterial physiology, host–microbe interactions and plant disease control.

  • Pseudomonas fluorescens
  • lipopeptides
  • antimicrobial
  • plant-microbe interactions
  • direct antagonism
  • induced systemic resistance
  • secondary metabolites

1. Introduction

The Pseudomonas genus is ubiquitous and comprises species which are well known phytopathogens, such as P. syringae, or opportunistic human pathogens, such as P. aeruginosa, but also host members associated with water, soil and plant surfaces [1]. Pseudomonas spp. are well adapted to growing in the rhizosphere and are well suited for biocontrol and growth promotion [2]. Thus, the use of fluorescent Pseudomonas spp. as potential biopesticides has gained attention over the last decade. These bacteria are of particular interest because of their enormous metabolic versatility and wide adaptation across environmental gradients [3].
Based on phylogenomic and Multi Locus Sequence Analyses (MLSA), the Pseudomonas genus has been delineated into 453 species (https://lpsn.dsmz.de/genus/pseudomonas; accessed on 18 December 2021) which are distributed across three lineages (P. fluorescens, P. aeruginosa and P. pertucinogena), several groups (G) and subgroups (SG) [4][5][6][7][8]. Most biocontrol strains have been described within the P. fluorescens group comprising among others, the P. fluorescens SG, P. koreensis SG, P. chlororaphis SG, P. jessenii SG, P. mandelii SG and P. corrugata SG. Additionally, several biocontrol strains are positioned within the P. putida and P. syringae groups. These disease-suppressing pseudomonads were isolated from several sources ranging from the healthy plant rhizosphere [9][10][11], plant rhizosphere [12][13][14][15], phyllosphere [16][17], bulk soil [15] and suppressive soils [10][18]. The commonality among well-studied biocontrol strains is their capacity for secondary metabolite production including siderophores, lipopeptides (LPs), hydrogen cyanide, bacteriocins and certain antibiotics such as phenazines, 2,4-diacetylphloroglucinol (DAPG), pyrrolnitrin and pyoluteorin [3][19].
Examples of commercially available Pseudomonas-based bioprotectants include fungicides such as Cedomon and Cerall (P. chlororaphis MA342) both targeting seed-borne pathogens of cereals, Spot-Less (P. aureofaciens strain Tx-1) for management of fungal diseases on lawns and grasses, and Howler (P. chlororaphis AFS009) useful in the management of Rhizoctonia, Pythium, Fusarium, Phytophthora, Colletotrichum spp. in fruits, vegetables and ornamentals [19]. A detailed list of commercial bioprotectants based on Pseudomonas in Europe and USA, including their usage, and target crops/applications/pathogens have been enumerated in a recent review [19].
Lipopeptides are bacterial metabolites consisting of a peptide part attached to a fatty acid tail [1]. Most beneficial LPs are cyclized although linear LPs have also been described [20][21]. LPs have drawn remarkable interest because of their broad-spectrum antimicrobial and ecological functions. These multiple functions include biofilm formation and colonization of surfaces, quorum sensing, cell motility, soil remediation, anti-oomycete, antiviral, antifungal, antibacterial, herbicidal, insecticidal, antiprotozoal and anticancer properties [3][22][23][24][25][26][27].

2. Genome Comparison of Selected Lipopeptide-Producing Pseudomonas spp.

A previous study provided the phylogenomic analysis of the Pseudomonas genus based on the genomes of the type strains of 163 described species and compared these type strain genomes to those of 1223 Pseudomonas genomes in public databases [7]. Results showed that 400 of those 1223 genomes were distinct from any other type strain suggesting that the Pseudomonas genomic diversity had been grossly underrepresented by the type strains. Furthermore, a detailed comparative genome analysis of ten strains within the Pseudomonas fluorescens group highlighted the enormous diverseness of this group and the capacity of the variable genome to adapt individual strains to their distinct lifestyles and functional capacities [3]. Here, using the P. fluorescens Pf0-1 as a reference genome, andwe compared the genome of 32 lipopeptide-producing Pseudomonas strains affiliated with the P. koreensis, P. fluorescens, P. mandelii, P. corrugata, P. asplenii, P. chlororaphis, P. protegens, subgroups including the P. putida and P. syringae groups. By comparing the protein coding sequences (CDS) of reference to query genomes, a Blast Atlas was generated which showed the close relatedness of other members of the P. koreensis group (P. fluorescens MS80, P. granadensis LMG 27,940 and P. kribbensis 46-2) to the reference genome P. fluorescens Pf0-1 (Figure 3).
Molecules 27 00372 g003 550
Figure 3. Comparative Genome Blast Atlas of 35 Lipopeptide-Producing Pseudomonas Strains. The BLAST Atlas analysis displays regions of the uploaded query files (34 genomes) where there are BLAST hits to the reference genome P. fluorescens Pf0-1). The GView Server was used [28].

3. Chemical Diversity of Beneficial Pseudomonas LPs

Most beneficial LPs have been predominantly characterized from strains affiliated with the P. fluorescens and P. putida group. The chemical diversity of Pseudomonas LPs has been detailed in two recent reviews [1][21]. Table 1 shows the diversity of beneficial LPs and presents the discovery of similar LPs from diverse strains, countries, niches and environments. Not all LPs listed have been functionally characterized, however, the disease suppressive capacity of their producing strain(s) has been established on specific plant hosts thus indicating non-virulence. Clearly, the P. koreensis subgroup presents the highest diversity of LP families and individual members, including variants. This SG is characterized by at least six amphisin group members alongside the novel rhizoamide, the bananamide group comprising six variants and the cocoyamide/gacamide group. Moderate LP diversity is showcased by the P. fluorescens SG while the P. protegens SG comprises various orfamide variants A-H and the poaeamide LPs. Lastly, the P. putida group contains four described LP types: entolysin, putisolvin, xantholysin, WLIP and a novel 17AA LP named N8. Figure 4 shows the chemical structures of representative biocontrol LPs that have been characterized.
Molecules 27 00372 g004 550
Figure 4. Chemical structures of selected biologically active Pseudomonas Cyclic Lipopeptides. Bananamide D (Bananamide Group); WLIP (Viscosin Group); Thanamycin (Syringomycin Group); Lokisin (Amphisin Group); Cocoyamide; Putisolvin I; Entolysin A and Xantholysin A. Whenever the absolute configuration of the lipopeptides was reported in the literature, it is indicated by standard stereodescriptors. In case of WLIP, the 3D-structure was secured by x-ray [29] and can be viewed as entry CCDC 919,229 at The Cambridge Crystallographic Data Centre via www.ccdc.cam.ac.uk (accessed on 19 December 2021).
Table 1. Taxonomy of LP-producing Biocontrol Pseudomonads, their corresponding Molecules and Origin.
Taxonomy Biocontrol Strains Host/Origin Country LP Family LP Reference
P. fluorescens SG SS101 Wheat rhizosphere Netherlands Viscosin Massetolide [30]
  SBW25 Sugarbeet phyllosphere UK   Viscosin [31]
  DR54 Sugarbeet rhizosphere Denmark   Viscosinamide [32][33]
  A2W4.9, U2W1.5 White cocoyam rhizosphere Nigeria   Viscosinamide [34]
  BRG100 Green foxtail rhizosphere Canada   Pseudophomin [35]
  RE*1-1-14 Internal part of soybean roots Germany   Poaemide [36][37]
  NCPPB1311 Cultivated mushrooms UK   WLIP [38]
P. koreensis SG DSS73 Sugarbeet rhizosphere Denmark Amphisin Amphisin [14][39]
  HKI0770 Forest soil Forest soil   Anikasin [40][41]
  CTS17 Sugarbeet rhizosphere Denmark   Hodersin [14][42]
  DSS41 Sugarbeet rhizosphere Denmark   Lokisin [43]
  2.74 Tomato hydroponics Sweden   Lokisin [44]
  S150 Tobacco rhizosphere China   Lokisin [45]
  COR10 Red cocoyam rhizosphere Cameroon   Lokisin [10]
  UCMA 17988 Raw bulk tank milk France   Milkisin [46]
  COW8 White cocoyam rhizosphere Cameroon   Rhizoamide (N2—11:7) † [11]
  96.578 Sugarbeet rhizosphere Denmark   Tensin [33][47]
  BW11P2 Banana rhizoplane Sri Lanka Bananamide Bananamide I, II, III [12][48]
  COW3, COW65 White cocoyam rhizosphere Cameroon   Bananamide D, E, F, G [10][49]
  COW5 White cocoyam rhizosphere Cameroon Cocoyamide Cocoyamide A [10]
  Pf0-1 Loam soil USA   Gacamide A [50][51]
P. protegens SG CHA0 Tobacco roots Switzerland Orfamide Orfamide [52][53]
  Pf-5 Cotton rhizosphere USA   Orfamide [54][55]
  CMR5c Red cocoyam rhizosphere Cameroon   Orfamide [53]
  CMR12a Red cocoyam rhizosphere Cameroon   Orfamide, Sessilin [56]
P. chlororaphis SG COR52 Red cocoyam rhizosphere Cameroon Viscosin Pseudodesmin [34]
P. mandelii SG In5 Suppressive potato soil Greenland Syringomycin Nunamycin [18]
  In5 Suppressive potato soil Greenland Syringopeptin Nunapeptin [18]
P. corrugata SG SH-C52 Sugarbeet rhizosphere Netherlands Syringomycin Thanamycin [57]
  DF41 Canola root Canada   Thanamycin -var1 [58][59]
  11K1 Bean rhizosphere China   Brasmycin [60]
  SH-C52 Sugarbeet rhizosphere Netherlands Syringopeptin Thanapeptin [57]
  DF41 Canola root Canada   Sclerosin [59]
  11K1 Bean rhizosphere China   Braspeptin [60]
P. putida G BW11M1 Banana rhizoplane Sri Lanka Xantholysin Xantholysin [12][61]
  COR51 Red cocoyam rhizosphere Cameroon   Xantholysin [10]
  BS011 Rice rhizosphere China   Xantholysin [62]
  267 Black pepper Vietnam Putisolvin Putisolvin I, II [63]
  COR55 Red cocoyam rhizosphere Cameroon   Putisolvin III, IV, V [10][11]
  L48 Fly Guadeloupe Entolysin Entolysin A, B [64]
  COR5 Red cocoyam rhizosphere Cameroon   Entolysin B [10]
  RW10S2 Rice rhizosphere Sri Lanka Viscosin WLIP [65]
  COW10 White cocoyam rhizosphere Cameroon   WLIP [10]
  NSE1 White cocoyam rhizosphere Nigeria   WLIP [66]
  COR35 Red cocoyam rhizosphere Cameroon Unclassified N8 (17:8) † [11]
P. asplenii SG COR33 Red cocoyam rhizosphere Cameroon Unclassified N5 (13:8) † [11]
  COR18 Red cocoyam rhizosphere Cameroon   N5 (13:8), N7 †, Mycin LP † [11]
Novel U2 SG COR58 Red cocoyam rhizosphere Cameroon Unclassified N4 (12:10) † [10][11]
† novel LPs.

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