Johan H J Leveau

University of California, Davis | UCD · Department of Plant Pathology

Conventional washing and sanitizing approaches for leafy greens provide limited inactivation of bacteria on leaf surfaces. For a quantitative understanding of the barriers to bacterial inactivation on leaf surfaces, this study develops a numerical simulation approach based on mass transport and surface reaction kinetics. Two specific sections of a...

The fungal genus Fusarium contains plant pathogens, mutualists, and commensalists. As non-pathogenic Fusarium strains can contribute to disease-suppression in soil by competition or induced plant resistance, identifying factors that influence the abundance of non-pathogenic strains could lead to strategies that enhance plant-beneficial interactions...

A key challenge in microbiome science is the scale mismatch problem, which arises when the scale at which microbial communities are sampled, interrogated, and averaged is different from the scale at which individual microorganisms within those communities interact with each other and with their environment. Profiling the microbial communities in a...

This study investigates methods to commercialize safer alternatives to chemical pesticides that pose risks to human safety and the environment. Spray-drying encapsulation of the plant-protective, antifungal bacterium Collimonas arenae Cal35 in in situ cross-linked alginate microcapsules (CLAMs) was optimized to minimize losses during spray-drying a...

Bacillus cereus is a common food-borne pathogen that is responsible for important outbreaks of food poisoning in humans. Diseases caused by B. cereus usually exhibit two major symptoms, emetic or diarrheic, depending on the toxins produced. It is assumed that after the ingestion of contaminated vegetables or processed food, spores of enterotoxigeni...

Bacillus cereus is a common food-borne pathogen that is responsible for important outbreaks of food poisoning in humans. Diseases caused by B. cereus usually exhibit two major symptoms, emetic or diarrheic, depending on the toxins produced. It is assumed that after the ingestion of contaminated vegetables or processed food, spores of enterotoxigeni...

In greenhouse and field trials, a bacterial mixture of Collimonas arenae Cal35 and Bacillus velezensis FZB42, but not Cal35 alone or FZB42 alone, was able to protect tomato plants from challenge with the soilborne fungal pathogen Fusarium oxysporum f.sp. lycopersici (Fol). To identify genes and mechanisms underlying this property in Cal35, we scree...

Indole-3-acetic acid (IAA) is a molecule with the chemical formula C10H9NO2, with a demonstrated presence in various environments and organisms, and with a biological function in several of these organisms, most notably in plants where it acts as a growth hormone. The existence of microorganisms with the ability to catabolize or assimilate IAA has...

The attachment of foodborne pathogens to leaf surfaces is a complex process that involves multiple physical, chemical, and biological factors. Here, we report the results from a study designed to specifically determine the contribution of spinach leaf surface topography as it relates to leaf axis (abaxial and adaxial) and leaf age (15, 45, and 75 d...

To study the impact of lateral variation in surface topography on the microbial colonization of plant leaves, we used a two-step casting process to generate topomimetic “replicasts” in polydimethylsiloxane which faithfully resembled leaf surface topography at submicrometer scale. This process revealed that the shape and size of the phyllotelma—the...

The plant leaf surface, or phyllosphere, represents a unique and challenging microbial biome with a diverse and dynamic community of commensal, parasitic, and mutualistic agents of microscopic proportions. This mini-review offers a digest of recently published research dedicated to the study of phyllosphere microbiota, framed in the context of proc...

Asymptomatic plant colonization is hypothesized to enhance persistence of pathogenic forms of Fusarium oxysporum. However, a correlation between pathogen populations on living, asymptomatic plant tissues and soilborne populations after tillage has not been demonstrated. Living and dead tissues of broccoli, lettuce, spinach, wheat, cilantro, raspber...

Asymptomatic plant colonization is hypothesized to enhance persistence of pathogenic forms of Fusarium oxysporum in the absence of a susceptible host. However, a correlation between pathogen populations on living plant tissues and soilborne populations after tillage has not been demonstrated. Living and dead tissues of broccoli, lettuce, spinach, w...

We report the results of a 3-year study in which we collected and analyzed soil and yield data from experimental plots in six commercial processing tomato fields in Yolo and Solano counties in California. Our objective was to assess the effect of soil chemistry and soil-delivered nutrients and fungicides on tomato plant health and fruit yield at ha...

Understanding how soil pedogenesis affects microbial communities and their in situ activities according to ecosystem functioning is a central issue in soil microbial ecology, as soils represent essential nutrient reservoirs and habitats for the biosphere. To address this question, soil chronosequences developed from a single, shared mineralogical p...

Models are important tools in microbial ecology. They can be used to advance understanding by helping to interpret observations and test hypotheses, and to predict the effects of ecosystem management actions or a different climate. Over the past decades, biological knowledge and ecosystem observations have advanced to the molecular and in particula...

Xanthomonas fragariae is a foliar pathogen of strawberry that is of significant concern to nursery production of strawberry transplants and field production of strawberry fruit. Long-read sequencing was employed to generate finished genomes for two isolates (each with one chromosome and two plasmids) from symptomatic plants in northern California.

In commercial production settings, few options exist to prevent or treat angular leaf spot (ALS) of strawberry, a disease of economic importance and caused by the bacterial pathogen Xanthomonas fragariae. In the process of isolating and identifying X. fragariae bacteria from symptomatic plants, we observed growth inhibition of X. fragariae by bacte...

Microorganisms are capable of remarkable social behaviours, such as forming transient multicellular assemblages with properties and adaptive abilities exceeding those of individual cells. Here, we report on the formation and structure of genets known as symplasmata produced by Pantoea eucalypti bacteria. Each symplasmatum develops clonally and stoc...

The impacts of plant species on the microbial communities and physico-chemical characteristics of soil are well documented for many herbs, grasses and legumes but much less so for tree species. Here, we investigate by rRNA and ITS amplicon sequencing the diversity of microorganisms from the three domains of life (Archaea, Bacteria and Eukaryota:Fun...

The phyllosphere, or leaf environment, is a temporally erratic, spatially heterogeneous, and inherently transient habitat that supports a large and diverse population of microorganisms. This chapter offers an introductory exploration of the leaf surface as a microbial biome and of the genes and gene functions that underlie the unique adaptations fo...

Modeling has become an important tool for widening our understanding of microbial growth in the context of applied microbiology and related to such processes as safe food production, wastewater treatment, bioremediation, or microbe-mediated mining. Various modeling techniques, such as primary, secondary and tertiary mathematical models, phenomenolo...

The study of microorganisms that reside on plant leaf surfaces, or phyllosphere microbiology, greatly benefits from the availability of artificial surfaces that mimic in one or more ways the complexity of foliage as a microbial habitat. These leaf surface proxies range from very simple, such as nutrient agars that can reveal the metabolic versatili...

We announce the finished genome sequence of soil forest isolate Collimonas arenae Cal35, which comprises a 5.6-Mbp chromosome and 41-kb plasmid. The Cal35 genome is the second one published for the bacterial genus Collimonas and represents the first opportunity for high-resolution comparison of genome content and synteny among collimonads.

Ectomycorrhizal fungi are surrounded by bacterial communities with which they interact physically and metabolically during their life cycle. These bacteria can have positive or negative effects on the formation and the functioning of ectomycorrhizae. However, relatively little is known about the mechanisms by which ectomycorrhizal fungi and associa...

The antifungal activity of bacteria from the genus Collimonas has been well documented, but the chemistry and gene functions that underlie this phenotype are still poorly understood. Screening of a random plasposon insertion library of Collimonas fungivorans Ter331 for loss-of-function mutants revealed the importance of gene cluster K, which is ann...

Microbial life on plant leaves is characterized by a multitude of interactions between leaf colonizers and their environment. While the existence of many of these interactions has been confirmed, their spatial scale or reach often remained unknown. In this study, we applied spatial point pattern analysis to 244 distribution patterns of Pantoea aggl...

Arthrobacter chlorophenolicus A6 is a Gram-positive, 4-chlorophenol degrading soil bacterium that was recently shown to be an effective colonizer of plant leaf surfaces. The genetic basis for this phyllosphere competency is unknown. In this paper, we describe the genome-wide expression profile of A. chlorophenolicus on leaves of common bean (Phaseo...

Progress in microbiology has always been driven by technological advances, ever since Antonie van Leeuwenhoek discovered bacteria by making an improved compound microscope. Yet until very recently, we have not been able to identify microbes and record their mostly invisible activities such as nutrient consumption or toxin production on the level of...

We developed the individual-based model PHYLLOSIM to explain observed variation in the size of bacterial clusters on plant leaf surfaces (the phyllosphere). Specifically, we tested how different 'waterscapes' impacted the diffusion of nutrients from the leaf interior to the surface and the growth of individual bacteria on these nutrients. In the 'n...

A genome-wide transcriptional profile of Bradyrhizobium japonicum, the nitrogen-fixing endosymbiont of the soybean plant, revealed differential expression of approximately 15% of the genome after a 1 mM treatment with the phytohormone indole-3-acetic acid (IAA). A total of 1,323 genes were differentially expressed (619 up-regulated and 704 down-reg...

The phyllosphere is an ecologically and economically important ecosystem that hosts a large and diverse microbial community. Phyllosphere microbiota play a critical role in protecting plants from diseases as well as promoting their growth by various mechanisms. There are serious gaps in our understanding of how and why microbiota composition varies...

Pseudomonas putida 1290 is a model organism for the study of bacterial degradation of the plant hormone indole-3-acetic acid (IAA). This property is encoded by the iac gene cluster. Insertional inactivation and/or deletion of individual iac genes and heterologous expression of the gene cluster in Escherichia coli were combined with mass spectrometr...

(A) Deconvoluted mass spectrum of compound #1 (top) and Binbase library spectrum for 5-hydroxyindole-3-acetic acid (bottom); ion peaks at m/z 290, 407 and 202 were used for putative annotation. (B) Deconvoluted mass spectrum of compound #2, putatively dioxindole-3-acetic acid, could not be annotated or identified using BinBase library; signature io...

GC-MS ion counts of indole-3-acetic acid (IAA) (blue), compound #1 (red), compound #2 (green), and catechol (purple, compound #3) in the supernatants of Escherichia coli TOP10 cultures grown overnight on M9 glucose medium supplemented with 0.2 mM IAA and carrying plasmid pIAC115-iacE::Tn5, -iacC::Tn5, -iacAB, -vector::Tn5, or -Δiac. ‘IAA Alone’ is...

We assessed how preemptive inoculation of plant leaves with bacteria affected the establishment of secondary colonizers. We quantified the latter in two ways: (i) at the population level, i.e. as counts of colony-forming units and (ii) at the level of single cells by tracking the reproductive success of individual bacteria. Both analyses showed tha...

Bacteria of the genus Arthrobacter are common inhabitants of the soil environment, but can also be recovered from leaf surfaces (the phyllosphere). Using enrichment cultures on 4-chlorophenol, we succeeded in specifically isolating Arthrobacter bacteria from ground cover vegetation in an apple orchard. Based on 16S rRNA gene sequencing, the isolate...

Bacteria belonging to the genus are common colonizers of plant leaf surfaces. Here, we present the draft genome sequence of 299R, a phyllosphere isolate that has become a model strain for studying the ecology of plant leaf-associated bacterial commensals.

Collimonas is a genus of soil bacteria comprising three recognized species: C. fungivorans, C. pratensis and C. arenae. Collimonads share the ability to degrade chitin (chitinolysis), feed on living fungal hyphae (mycophagy), and dissolve minerals (weathering), but vary in their inhibition of fungi (fungistasis). To better understand this phenotypi...

We demonstrate that the term ‘carrying capacity’, as it is commonly used in microbial ecology, needs to be understood as the sum of ‘local carrying capacities’ to better explain and predict the course and outcome of bacterial colonization of an environment. By reconstructing the contribution of individual bacterial immigrants to observed changes of...

The presence, size and importance of bacterial communities on plant leaf surfaces are widely appreciated. However, information is scarce regarding their composition and how it changes along geographical and seasonal scales. We collected 106 samples of field-grown Romaine lettuce from commercial production regions in California and Arizona during th...

Many concepts and theories in ecology are highly debated, because it is often difficult to design decisive tests with sufficient replicates. Examples include biodiversity theories, succession concepts, invasion theories, coexistence theories, and concepts of life history strategies. Microbiological tests of ecological concepts are rapidly accumulat...

Bacteria that colonize the leaves of terrestrial plants often occur in clusters whose size varies from a few to thousands of cells. For the formation of such bacterial clusters, two non-mutually exclusive but very different mechanisms may be proposed: aggregation of multiple cells or clonal reproduction of a single cell. Here we assessed the contri...

Using a phyllosphere model system, we demonstrated that the term 'carrying capacity', as it is commonly used in microbial ecology, needs to be understood as the sum of many 'local carrying capacities' in order to better explain and predict the course and outcome of bacterial colonization of an environment. Using a green fluorescent protein-based bi...

This review by a multidisciplinary team maps key components and emerging connections within the intellectual landscape of agroecology. We attempt to extend and preview agroecology as a discipline in which agriculture can be conceptualized within the context of global change and studied as a coupled system involving a wide range of social and natura...

In phyllosphere microbiology, the distribution of resources available to bacterial colonizers of leaf surfaces is generally understood to be very heterogeneous. However, there is little quantitative understanding of the mechanisms that underlie this heterogeneity. Here, we tested the hypothesis that different parts of the cuticle vary in the degree...

We used the culture-independent method of high-throughput pyrosequencing of 16S ribosomal RNA (rRNA) gene amplicons to analyze the diversity of bacteria associated with the leaf and berry surfaces of 'Chardonnay' grape in a vineyard close to harvest. Combined, more than half of all bacterial sequences were classified as Proteobacteria. Other well-r...

Interactions between bacteria and fungi cover a wide range of incentives, mechanisms and outcomes. The genus Collimonas consists of soil bacteria that are known for their antifungal activity and ability to grow at the expense of living fungi. In non-contact confrontation assays with the fungus Aspergillus niger, Collimonas fungivorans showed accumu...

On plants, microbial populations interact with each other and their host through the actions of secreted metabolites. However, the combined action of diverse organisms and their different metabolites on plant health has yet to be fully appreciated. Here, the multifactorial nature of these interactions, at the organismal and molecular level, leading...

A major obstacle in the culture-independent estimation of the abundance of bacteria associated with plants is contamination with plant organelles, which precludes the use of universal rRNA bacterial primers in quantitative PCR applications. We present here a PCR-based method that allows a priori determination of the degree of chloroplast and mitoch...