The Pseudomonas syringae complex is composed of numerous genetic lineages of strains from both agricultural and environmental habitats including habitats closely linked to the water cycle. The new insights from the discovery of this bacterial species in habitats outside of agricultural contexts per se have led to the revelation of a wide diversity of strains in this complex beyond what was known from agricultural contexts. Here, through Multi Locus Sequence Typing (MLST) of 216 strains, we identified 23 clades within 13 phylogroups among which the seven previously described P. syringae phylogroups were included. The phylogeny of the core genome of 29 strains representing nine phylogroups was similar to the phylogeny obtained with MLST thereby confirming the robustness of MLST-phylogroups. We show that phenotypic traits rarely provide a satisfactory means for classification of strains even if some combinations are highly probable in some phylogroups. We demonstrate that the citrate synthase (cts) housekeeping gene can accurately predict the phylogenetic affiliation for more than 97% of strains tested. We propose a list of cts sequences to be used as a simple tool for quickly and precisely classifying new strains. Finally, our analysis leads to predictions about the diversity of P. syringae that is yet to be discovered. We present here an expandable framework mainly based on cts genetic analysis into which more diversity can be integrated.
Pseudomonas syringae is a plant pathogen well known for its capacity to grow epiphytically on diverse plants and for its ice-nucleation activity. The ensemble of its known biology and ecology led us to postulate that this bacterium is also present in non-agricultural habitats, particularly those associated with water. Here, we report the abundance of P. syringae in rain, snow, alpine streams and lakes and in wild plants, in addition to the previously reported abundance in epilithic biofilms. Each of these substrates harbored strains that corresponded to P. syringae in terms of biochemical traits, pathogenicity and pathogenicity-related factors and that were ice-nucleation active. Phylogenetic comparisons of sequences of four housekeeping genes of the non-agricultural strains with strains of P. syringae from disease epidemics confirmed their identity as P. syringae. Moreover, strains belonging to the same clonal lineage were isolated from snow, irrigation water and a diseased crop plant. Our data suggest that the different substrates harboring P. syringae modify the structure of the associated populations. Here, we propose a comprehensive life cycle for P. syringae-in agricultural and non-agricultural habitats-driven by the environmental cycle of water. This cycle opens the opportunity to evaluate the importance of non-agricultural habitats in the evolution of a plant pathogen and the emergence of virulence. The ice-nucleation activity of all strains from snow, unlike from other substrates, strongly suggests that P. syringae plays an active role in the water cycle as an ice nucleus in clouds.
Despite the integral role of ice nucleators (IN) in atmospheric processes leading to precipitation, their sources and distributions have not been well established. We examined IN in snowfall from mid- and high-latitude locations and found that the most active were biological in origin. Of the IN larger than 0.2 micrometer that were active at temperatures warmer than -7 degrees C, 69 to 100% were biological, and a substantial fraction were bacteria. Our results indicate that the biosphere is a source of highly active IN and suggest that these biological particles may affect the precipitation cycle and/or their own precipitation during atmospheric transport.
Landscapes influence precipitation via the water vapor and energy fluxes they generate. Biologically active landscapes also generate aerosols containing microorganisms, some being capable of catalyzing ice formation and crystal growth in clouds at temperatures near 0 °C. The resulting precipitation is beneficial for the growth of plants and microorganisms. Mounting evidence from observations and numerical simulations support the plausibility of a bioprecipitation feedback cycle involving vegetated landscapes and the microorganisms they host. Furthermore, the evolutionary history of ice nucleation-active bacteria such as Pseudomonas syringae supports that they have been part of this process on geological time scales since the emergence of land plants. Elucidation of bioprecipitation feedbacks involving landscapes and their microflora could contribute to appraising the impact that modified landscapes have on regional weather and biodiversity, and to avoiding inadvertent, negative consequences of landscape management.
Certain bacteria that are commonly found on plants have the capacity to catalyze the freezing of supercooled water at temperatures as warm as −1 • C. This is conferred by a protein in the outer membrane of the bacterial cell. Because of the abundance of these bacteria and the warm temperature at which they function as ice nuclei, they are considered to be among the most active of the naturally-occurring ice nuclei. As plant pathogens, antagonists of plant pathogens and as causal agents of frost damage, these bacteria have wellstudied interactions with plants. Here we propose that these bacteria also play a role in atmospheric processes leading to rain, given that they are readily disseminated into the atmosphere and have been found in clouds at altitudes of several kilometers. That they participate in a sort of biological cycle of precipitation-whereby they are transported into clouds from plant canopies and incite rain thereby causing favorable conditions for their growth on plant surfaces-was proposed about 20 years ago. Today, sufficient evidence and meteorological tools have emerged to re-ignite interest in bioprecipitation and in the ways in which plants play a role as cloud seeders. 88 JOURNAL DE PHYSIQUE IV 2. THE BIOLOGICAL COMPONENT OF AEROSOLS Outside of urban zones, the air over continents contains 3 × 10 9 to 5 × 10 10 particles/m 3. Mineral dusts are abundant in atmospheric aerosols. In polluted regions a major component of these aerosols can be soot. But, anyone afflicted with allergies to pollen knows that there is a biological component to atmospheric aerosols. In fact, up to 25 % of the insoluble part of aerosols can be of biological origin [1]. Pollen is only one of the biological components of aerosols and is only one of the types of particles that plants contribute to the atmosphere. The seemingly abiotic atmosphere that surrounds our planet is a bouillon of biological bits including bacteria; protozoa; spores of fungi, ferns and mosses; virus particles; parts of insects and dust mites; algae and pollen grains. In some cases, these biotic particles are dead debris that are picked up into the air. But often, aerial dissemination is an integral part of the life cycle of organisms, a sort of boulevard to opportunities for species out-crossing and to supplemental food and water resources. At altitudes below about 15 m, there are hundreds to thousands of particles of biological origin per m 3 of air. Over a suburban region the quantity of microorganisms, for example, in the air has been observed to be as high as 7000 culturable propagules of fungi and 1600 cultural bacteria/m 3 [2]. The bulk of the popular interest in aerobiology concerns the presence-in the air we breath-of biological particles with direct negative impacts on human health such as allergens, causal agents of pneumonia and other lung diseases and of septicemias in hospital environments. The Andersen sampler, widely used in studies of aerobiology, was conceived to simulate uptake of particles by the human respiratory system [3]. This...
Biological ice nucleators (IN) function as catalysts for freezing at relatively warm temperatures (warmer than ؊10°C).We examined the concentration (per volume of liquid) and nature of IN in precipitation collected from Montana and Louisiana, the Alps and Pyrenees (France), Ross Island (Antarctica), and Yukon (Canada). The temperature of detectable ice-nucleating activity for more than half of the samples was > ؊5°C based on immersion freezing testing. Digestion of the samples with lysozyme (i.e., to hydrolyze bacterial cell walls) led to reductions in the frequency of freezing (0 -100%); heat treatment greatly reduced (95% average) or completely eliminated ice nucleation at the measured conditions in every sample. These behaviors were consistent with the activity being bacterial and/or proteinaceous in origin. atmosphere ͉ climate ͉ microbial dissemination ͉ biological ice nuclei A t subzero temperatures warmer than Ϫ40°C, aerosol particles in clouds initiate freezing through the heterogeneous nucleation of ice directly from water vapor or by freezing droplets via several mechanisms: deposition, condensation, contact, and immersion freezing (1). These processes lead to ice formation in clouds that can trigger precipitation. A diverse range of natural and anthropogenic particles, referred to as ice-forming nuclei or ice nucleators (IN), are capable of initiating the ice phase (2). The maximum temperature at which an IN can initiate freezing is specific to that nucleator, but they function similarly by providing templates for the aggregation of individual water molecules in the configuration of an ice embryo, resulting in a subsequent phase change and the cascade of crystal formation (3). Consequently, knowledge of the nature and sources of IN in the atmosphere is important for understanding the meteorological processes responsible for precipitation. The most active naturally occurring IN are biological in origin and have the capacity to catalyze freezing at temperatures near Ϫ2°C (4). The most widespread and well-studied biological aerosols with icenucleating activity are comprised of certain species of plantassociated bacteria (Pseudomonas syringae, Pseudomonas viridiflava, Pseudomonas fluorescens, Pantoea agglomerans, and Xanthomonas campestris), but also fungi (e.g., Fusarium avenaceum), algae such as Chlorella minutissima, and birch pollen (5). P. syringae (6 -8) and F. avenaceum (7) in particular have been detected in atmospheric aerosols and clouds. Icenucleating strains of P. syringae possess a 120-to 180-kDa ice nucleation active protein in their outer membrane comprised of contiguous repeats of a consensus octapeptide; the protein binds water molecules in an ordered arrangement, providing a nucleating template that enhances ice crystal formation (9).Based on reports of ice-nucleating bacteria at altitudes of several kilometers (6, 10) and the warm temperatures at which they function as ice nuclei (Ϫ2°C to Ϫ7°C; ref. Our previous work on snowfall collected from a variety of midand high-latitude locations...
Nonhost environmental reservoirs of pathogens play key roles in their evolutionary ecology and in particular in the evolution of pathogenicity. In light of recent reports of the plant pathogen Pseudomonas syringae in pristine waters outside agricultural regions and its dissemination via the water cycle, we have examined the genetic and phenotypic diversity, population structure, and biogeography of P. syringae from headwaters of rivers on three continents and their phylogenetic relationship to strains from crops. A collection of 236 strains from 11 sites in the United States, in France, and in New Zealand was characterized for genetic diversity based on housekeeping gene sequences and for phenotypic diversity based on measures of pathogenicity and ice nucleation activity. Phylogenetic analyses revealed several new genetic clades from water. The genetic structure of P. syringae populations was not influenced by geographic location or water chemistry, whereas the phenotypic structure was affected by these parameters. Comparison with strains from crops revealed that the metapopulation of P. syringae is structured into three genetic ecotypes: a crop-specific type, a water-specific type, and an abundant ecotype found in both habitats. Aggressiveness of strains was significantly and positively correlated with ice nucleation activity. Furthermore, the ubiquitous genotypes were the most aggressive, on average. The abundance and diversity in water relative to crops suggest that adaptation to the freshwater habitat has played a nonnegligible role in the evolutionary history of P. syringae. We discuss how adaptation to the water cycle is linked to the epidemiological success of this plant pathogen.
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