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Insect Pathogenicity in Plant-Beneficial Pseudomonads: Phylogenetic Distribution and Comparative Genomics

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Insect Pathogenicity in Plant-Beneficial Pseudomonads: Phylogenetic Distribution and Comparative Genomics The ISME Journal (2016) 10, 2527–2542 © 2016 International Society for Microbial Ecology All rights reserved 1751-7362/16 www.nature.com/ismej ORIGINAL ARTICLE Insect pathogenicity in plant-beneficial pseudomonads: phylogenetic distribution and comparative genomics Pascale Flury1, Nora Aellen1, Beat Ruffner1, Maria Péchy-Tarr2, Shakira Fataar1, Zane Metla1,3, Ana Dominguez-Ferreras1, Guido Bloemberg4, Joachim Frey5, Alexander Goesmann6, Jos M Raaijmakers7, Brion Duffy8, Monica Höfte9, Jochen Blom6, Theo HM Smits8, Christoph Keel2 and Monika Maurhofer1 1Plant Pathology, Institute of Integrative Biology, ETH Zürich, Zürich, Switzerland; 2Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland; 3Laboratory of Experimental Entomology, Institute of Biology, University of Latvia, Riga, Latvia; 4Institute of Medical Microbiology, University of Zurich, Zürich, Switzerland; 5Institute of Veterinary Bacteriology, University of Bern, Bern, Switzerland; 6Bioinformatics and Systems Biology, Justus-Liebig-University Giessen, Giessen, Germany; 7Department of Microbial Ecology, Netherlands Institute of Ecology, NIOO-KNAW, Wageningen, The Netherlands; 8Environmental Genomics and Systems Biology Research Group, Institute for Natural Resource Sciences, Zürich University of Applied Sciences, Wädenswil, Switzerland and 9Laboratory of Phytopathology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties including pathogen suppression. Recent observations that some strains of this group also cause lethal infections in insect larvae, however, point to a more versatile ecology of these bacteria. We show that 26 P. fluorescens group strains, isolated from three continents and covering three phylogenetically distinct sub-clades, exhibited different activities toward lepidopteran larvae, ranging from lethal to avirulent. All strains of sub-clade 1, which includes Pseudomonas chlororaphis and Pseudomonas protegens, were highly insecticidal regardless of their origin (animals, plants). Comparative genomics revealed that strains in this sub-clade possess specific traits allowing a switch between plant- and insect-associated lifestyles. We identified 90 genes unique to all highly insecticidal strains (sub-clade 1) and 117 genes common to all strains of sub-clade 1 and present in some moderately insecticidal strains of sub-clade 3. Mutational analysis of selected genes revealed the importance of chitinase C and phospholipase C in insect pathogenicity. The study provides insight into the genetic basis and phylogenetic distribution of traits defining insecticidal activity in plant-beneficial pseudomonads. Strains with potent dual activity against plant pathogens and herbivorous insects have great potential for use in integrated pest management for crops. The ISME Journal (2016) 10, 2527–2542; doi:10.1038/ismej.2016.5; published online 19 February 2016 Introduction exhibiting a wide variety of ecological behaviors. Some are feared as human or plant pathogens Bacteria of the genus Pseudomonas occupy diverse such as Pseudomonas aeruginosa or Pseudomonas terrestrial, aquatic and atmospheric environments, syringae; others are welcome agents for bioremedia- tion of pollutants such as Pseudomonas putida. Correspondence: THM Smits, Environmental Genomics and Members of the Pseudomonas fluorescens group Systems Biology Research Group, Institute for Natural Resource are well-known for plant-beneficial effects that Sciences, Zürich University of Applied Sciences ZHAW, Postfach, improve crop health and agricultural production. Grüental, Wädenswil 8820, Switzerland. Many strains of fluorescent pseudomonads isolated E-mail: [email protected] or C Keel, Department of Fundamental Microbiology, University of from the rhizosphere have been studied for their Lausanne, Biophore Building, Lausanne CH-1015, Switzerland. ability to suppress root diseases, to promote plant E-mail: [email protected] growth and to induce systemic resistance (Haas and or M Maurhofer, Plant Pathology, Institute of Integrative Biology Défago, 2005; Bakker et al., 2007). They harbor ETH Zürich, Universitätstrasse 2, Zürich CH-8092, Switzerland. E-mail: [email protected] strain-specific arsenals of antifungal metabolites, Received 25 July 2015; revised 9 December 2015; accepted which enable them to inhibit pathogen growth 22 December 2015; published online 19 February 2016 through direct antibiosis (Haas and Keel, 2003; Insecticidal arsenal in plant pseudomonads P Flury et al 2528 Raaijmakers et al., 2010). All these features make D. melanogaster larvae, but to a much lower extent fluorescent pseudomonads interesting organisms for than P. protegens Pf-5 (Olcott et al., 2010). use as biofertilizers and biopesticides in sustainable The discovery of insecticidal activity in fluores- agriculture and several products have been commer- cent pseudomonads raises diverse ecological and cialized (Kupferschmied et al., 2013). On top of agronomic questions. What ecological advantage plant-beneficial activity, genomics has revealed may be gained by this ability to switch from a plant unexpected and broader ecological versatility for to an insect environment? Can we use these these bacteria (Paulsen et al., 2005; Loper et al., pseudomonads as double agents to fight both plant 2012). Three of the best-characterized biocontrol disease and insect pests? To date, our understanding strains, Pseudomonas protegens strains CHA0 and of the interaction of plant-associated pseudomonads Pf-5 and Pseudomonas chlororaphis PCL1391, were with insects is still very poor. Although large shown to have potent insecticidal activity (Péchy- differences in their ability to infect insects were Tarr et al., 2008; Ruffner et al., 2013). When injected found between the strains investigated so far, no into the hemocoel of Galleria mellonella or Manduca extensive data on frequency and distribution of sexta larvae, they rapidly multiply and cause larval insecticidal activity throughout the whole P. fluor- death within a few hours (Péchy-Tarr et al., 2008). escens group is available and individual strains with Ecologically more relevant, these strains are also able different phylogenetic background have never been to infect and kill insect larvae, such as Drosophila compared directly. Moreover, the precise factors melanogaster and the agricultural pests Spodoptera beyond the Fit toxin, which enable certain fluores- littoralis or Plutella xylostella, after oral uptake cent pseudomonads to kill insects, and thereby to (Olcott et al., 2010; Ruffner et al., 2013). Oral occupy a habitat alternative to plant roots, are still insecticidal activity is considered a rare trait elusive. As a first step toward understanding the amongst bacteria and requires specific mechanisms genomic features enabling insect pathogenicity we to cope with host immune responses and to breach have taken an approach that combines bioassays the gut epithelium in order to access the hemocoel with comparative genomics. We investigated 26 (Vallet-Gely et al., 2008; Opota et al., 2011; Herren strains of fluorescent pseudomonads for their insec- and Lemaitre, 2012). How P. protegens and ticidal activity and their biocontrol activity against P. chlororaphis overcome these barriers remains root diseases. The strains included in our study are unclear. However, an association with insecticidal representative of the three phylogenetic sub-clades activity has been demonstrated for a set of genes within the P. fluorescens group that harbor most termed the fit genes (P. fluorescens insecticidal plant-beneficial pseudomonads and were isolated toxin) (Péchy-Tarr et al., 2008; Péchy-Tarr et al., from root but also from non-root habitats. Strong oral 2013; Ruffner et al., 2013). The unique virulence activity was found for all strains belonging to the cassette harbors the fitD gene encoding the protei- phylogenetic sub-clade 1, which showed potent naceous Fit toxin as well as regulatory genes and a dual activity against insects and plant pathogens. type I secretion system (Péchy-Tarr et al., 2008; However, we identified also a second phylogenetic Péchy-Tarr et al., 2013; Kupferschmied et al., 2014). group, sub-clade 3, containing strains with lower Nevertheless, fitD deletion mutants retain substantial insecticidal activity. The strains were sequenced and toxicity, indicating the existence of additional comparative genomics revealed around 200 genes virulence factors (Péchy-Tarr et al., 2008; Ruffner that are common and unique to the insecticidal et al., 2013). Mutational analyses provide evidence strains and we hypothesize that this specific set of that some of them are regulated by the global genes may represent major evolutionary events regulator GacA (Olcott et al., 2010; Ruffner et al., toward insect pathogenicity of Pseudomonas spp. 2013). Finally, we present first results from testing the Insecticidal activity is not universal to the involvement of some of the newly identified putative P. fluorescens group. A survey by Ruffner et al. virulence factors in insecticidal activity using a (2015) revealed that sub-clade 2 strains (Loper et al., mutational approach. 2012) neither harbor fit genes nor have ability to kill G. mellonella larvae. In contrast, all tested P. protegens and P. chlororaphis strains, which Materials and methods represent the sub-clade 1 (Loper et al.,
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