Human Pathogens in Primary Production Systems

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Plant Microbe Interactions".

Deadline for manuscript submissions: closed (31 October 2021) | Viewed by 25272

Special Issue Editor


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Guest Editor
Plant Research International, Wageningen University and Research Centre, Wageningen, The Netherlands
Interests: ecology of human pathogens (including E. coli O157, E. coli O104 and Salmonella Typhimurium) in freshly consumable crop plants; metagenomics on nematode- (Pratylenchus penetrans) suppressive soils; endophytic colonization of plant (root) growth promoting micro-organisms; so called bio-effectors; drought tolerance in Gram-negative bacteria

Special Issue Information

Dear Colleagues,

Plants live in association with micro-organisms, and, occasionally, these micro-organisms show close taxonomical resemblance to micro-organisms that are potentially harmful to humans or are actual human pathogens. Not so much is known about these so-called presumptive human pathogens present in plants’ microbiomes. It is the aim of this Special Issue of Microorganisms to bring together original research papers and reviews on the topic of presumptive human pathogens in plant production systems. In particular, topics of interest of this Special Issue are presumptive human pathogens acting as ‘cross-kingdom hoppers’ between plants, animals, water, soil, and other ecosystems considered to be potential threats to human and animal health as well as the interaction between the microbiomes of plants and those of these other ecosystems relevant to plant production. This Special Issue arises from a collaboration within the European HUPLANT control network that is supported by EU COST. All manuscripts dealing with all kinds of presumptive pathogens occurring in plant production systems, such as fungi, bacteria, and viruses, or describing the potential threats they pose to humans, such as virulence traits, (antibiotic) resistance, and production of (myco-) toxins, are welcome.

Dr. Leonard S van Overbeek
Guest Editor

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Keywords

  • human pathogens
  • plant production system
  • plant microbiome
  • plant–microbe interaction
  • ecosystem

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Published Papers (8 papers)

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Editorial

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3 pages, 182 KiB  
Editorial
Human Pathogens in Primary Production Systems
by Leo van Overbeek
Microorganisms 2023, 11(3), 750; https://doi.org/10.3390/microorganisms11030750 - 14 Mar 2023
Cited by 1 | Viewed by 1427
Abstract
Human pathogenic micro-organisms can contaminate plants [...] Full article
(This article belongs to the Special Issue Human Pathogens in Primary Production Systems)

Research

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11 pages, 1398 KiB  
Communication
Exploring Mitogenomes Diversity of Fusarium musae from Banana Fruits and Human Patients
by Luca Degradi, Valeria Tava, Anna Prigitano, Maria Carmela Esposto, Anna Maria Tortorano, Marco Saracchi, Andrea Kunova, Paolo Cortesi and Matias Pasquali
Microorganisms 2022, 10(6), 1115; https://doi.org/10.3390/microorganisms10061115 - 28 May 2022
Cited by 2 | Viewed by 2203
Abstract
Fusarium musae has recently been described as a cross-kingdom pathogen causing post-harvest disease in bananas and systemic and superficial infection in humans. The taxonomic identity of fungal cross-kingdom pathogens is essential for confirming the identification of the species on distant infected hosts. Understanding [...] Read more.
Fusarium musae has recently been described as a cross-kingdom pathogen causing post-harvest disease in bananas and systemic and superficial infection in humans. The taxonomic identity of fungal cross-kingdom pathogens is essential for confirming the identification of the species on distant infected hosts. Understanding the level of variability within the species is essential to decipher the population homogeneity infecting human and plant hosts. In order to verify that F. musae strains isolated from fruits and patients are part of a common population and to estimate their overall diversity, we assembled, annotated and explored the diversity of the mitogenomes of 18 F. musae strains obtained from banana fruits and human patients. The mitogenomes showed a high level of similarity among strains with different hosts’ origins, with sizes ranging from 56,493 to 59,256 bp. All contained 27 tRNA genes and 14 protein-coding genes, rps3 protein, and small and large ribosomal subunits (rns and rnl). Variations in the number of endonucleases were detected. A comparison of mitochondrial endonucleases distribution with a diverse set of Fusarium mitogenomes allowed us to specifically discriminate F. musae from its sister species F. verticillioides and the other Fusarium species. Despite the diversity in F. musae mitochondria, strains from bananas and strains from human patients group together, indirectly confirming F. musae as a cross-kingdom pathogen. Full article
(This article belongs to the Special Issue Human Pathogens in Primary Production Systems)
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17 pages, 1371 KiB  
Article
Transmission of Escherichia coli from Manure to Root Zones of Field-Grown Lettuce and Leek Plants
by Leo van Overbeek, Marie Duhamel, Stefan Aanstoot, Carin Lombaers van der Plas, Els Nijhuis, Leo Poleij, Lina Russ, Patricia van der Zouwen and Beatriz Andreo-Jimenez
Microorganisms 2021, 9(11), 2289; https://doi.org/10.3390/microorganisms9112289 - 3 Nov 2021
Cited by 9 | Viewed by 2499
Abstract
Pathogenic Escherichia coli strains are responsible for food-borne disease outbreaks upon consumption of fresh vegetables and fruits. The aim of this study was to establish the transmission route of E. coli strain 0611, as proxy for human pathogenic E. coli, via manure, [...] Read more.
Pathogenic Escherichia coli strains are responsible for food-borne disease outbreaks upon consumption of fresh vegetables and fruits. The aim of this study was to establish the transmission route of E. coli strain 0611, as proxy for human pathogenic E. coli, via manure, soil and plant root zones to the above-soil plant compartments. The ecological behavior of the introduced strain was established by making use of a combination of cultivation-based and molecular targeted and untargeted approaches. Strain 0611 CFUs and specific molecular targets were detected in the root zones of lettuce and leek plants, even up to 272 days after planting in the case of leek plants. However, no strain 0611 colonies were detected in leek leaves, and only in one occasion a single colony was found in lettuce leaves. Therefore, it was concluded that transmission of E. coli via manure is not the principal contamination route to the edible parts of both plant species grown under field conditions in this study. Strain 0611 was shown to accumulate in root zones of both species and metagenomic reads of this strain were retrieved from the lettuce rhizosphere soil metagenome library at a level of Log 4.11 CFU per g dry soil. Full article
(This article belongs to the Special Issue Human Pathogens in Primary Production Systems)
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17 pages, 944 KiB  
Article
Identification and Characterization of 33 Bacillus cereus sensu lato Isolates from Agricultural Fields from Eleven Widely Distributed Countries by Whole Genome Sequencing
by Athanasios Zervas, Marie Rønne Aggerbeck, Henrietta Allaga, Mustafa Güzel, Marc Hendriks, IIona Jonuškienė, Orsolya Kedves, Ayse Kupeli, Janja Lamovšek, Pascal Mülner, Denise Munday, Şahin Namli, Hilal Samut, Ružica Tomičić, Zorica Tomičić, Filiz Yeni, Raida Zribi Zghal, Xingchen Zhao, Vincent Sanchis-Borja and Niels Bohse Hendriksen
Microorganisms 2020, 8(12), 2028; https://doi.org/10.3390/microorganisms8122028 - 18 Dec 2020
Cited by 11 | Viewed by 4340
Abstract
The phylogeny, identification, and characterization of 33 B. cereus sensu lato isolates originating from 17 agricultural soils from 11 countries were analyzed on the basis of whole genome sequencing. Phylogenetic analyses revealed all isolates are divided into six groups, which follows the generally [...] Read more.
The phylogeny, identification, and characterization of 33 B. cereus sensu lato isolates originating from 17 agricultural soils from 11 countries were analyzed on the basis of whole genome sequencing. Phylogenetic analyses revealed all isolates are divided into six groups, which follows the generally accepted phylogenetic division of B. cereus sensu lato isolates. Four different identification methods resulted in a variation in the identity of the isolates, as none of the isolates were identified as the same species by all four methods—only the recent identification method proposed directly reflected the phylogeny of the isolates. This points to the importance of describing the basis and method used for the identification. The presence and percent identity of the protein product of 19 genes potentially involved in pathogenicity divided the 33 isolates into groups corresponding to phylogenetic division of the isolates. This suggests that different pathotypes exist and that it is possible to differentiate between them by comparing the percent identity of proteins potentially involved in pathogenicity. This also reveals that a basic link between phylogeny and pathogenicity is likely to exist. The geographical distribution of the isolates is not random: they are distributed in relation to their division into the six phylogenetic groups, which again relates to different ecotypes with different temperature growth ranges. This means that we find it easier to analyze and understand the results obtained from the 33 B. cereus sensu lato isolates in a phylogenetic, patho-type and ecotype-oriented context, than in a context based on uncertain identification at the species level. Full article
(This article belongs to the Special Issue Human Pathogens in Primary Production Systems)
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17 pages, 2207 KiB  
Article
The Role of Pea (Pisum sativum) Seeds in Transmission of Entero-Aggregative Escherichia coli to Growing Plants
by Leonard S. van Overbeek, Carin Lombaers-van der Plas and Patricia van der Zouwen
Microorganisms 2020, 8(9), 1271; https://doi.org/10.3390/microorganisms8091271 - 21 Aug 2020
Cited by 6 | Viewed by 2504
Abstract
Crop plants can become contaminated with human pathogenic bacteria in agro-production systems. Some of the transmission routes of human pathogens to growing plants are well explored such as water, manure and soil, whereas others are less explored such as seeds. Fenugreek seeds contaminated [...] Read more.
Crop plants can become contaminated with human pathogenic bacteria in agro-production systems. Some of the transmission routes of human pathogens to growing plants are well explored such as water, manure and soil, whereas others are less explored such as seeds. Fenugreek seeds contaminated with the entero-hemorrhagic Escherichia coli O104:H4 were suspected to be the principle vectors for transmission of the pathogen to sprouts at the food-borne disease outbreak in Hamburg and surrounding area in 2011. In this study we raised the questions of whether cells of the entero-aggregative E. coli O104:H4 strain 55989 is capable of colonizing developing plants from seeds and if it would be possible that, via plant internalization, these cells can reach the developing embryonic tissue of the next generation of seeds. To address these questions, we followed the fate of strain 55989 and of two other E. coli strains from artificially contaminated seeds to growing plants, and from developing flower tissue to mature seeds upon proximate introductions to the plant reproductive organs. Escherichia coli strains differing in origin, adherence properties to epithelial cells, and virulence profile were used in our experimentation to relate eventual differences in seed and plant colonization to typical E. coli properties. Experiments were conducted under realistic growth circumstances in greenhouse and open field settings. Entero-aggregative E. coli strain 55989 and the two other E. coli strains were able to colonize the root compartment of pea plants from inoculated seeds. In roots and rhizosphere soil, the strains could persist until the senescent stage of plant growth, when seeds had ripened. Colonization of the above-soil parts was only temporary at the start of plant growth for all three E. coli strains and, therefore, the conclusion was drawn that translocation of E. coli cells via the vascular tissue of the stems to developing pea seeds seems unlikely under circumstances realistic for agricultural practices. Proximate introductions of cells of E. coli strains to developing flowers also did not result in internal seed contamination, indicating that internal seed contamination with E. coli is an unlikely event. The fact that all three E. coli strains showed stronger preference for the root-soil zones of growing pea plants than for the above soil plant compartments, in spite of their differences in clinical behaviour and origin, indicate that E. coli in general will colonize root compartments of crop plants in production systems. Full article
(This article belongs to the Special Issue Human Pathogens in Primary Production Systems)
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15 pages, 1702 KiB  
Article
Composted Sewage Sludge Influences the Microbiome and Persistence of Human Pathogens in Soil
by Nikola Major, Jasper Schierstaedt, Sven Jechalke, Joseph Nesme, Smiljana Goreta Ban, Marko Černe, Søren J. Sørensen, Dean Ban and Adam Schikora
Microorganisms 2020, 8(7), 1020; https://doi.org/10.3390/microorganisms8071020 - 9 Jul 2020
Cited by 21 | Viewed by 4036
Abstract
Composted sewage sludge (CSS) gained attention as a potential fertilizer in agriculture. Application of CSS increases soil microbial activity and microbial biomass, however, it can also lead to increased chemical and microbiological risks. In this study, we performed microcosm experiments to assess how [...] Read more.
Composted sewage sludge (CSS) gained attention as a potential fertilizer in agriculture. Application of CSS increases soil microbial activity and microbial biomass, however, it can also lead to increased chemical and microbiological risks. In this study, we performed microcosm experiments to assess how CSS reshapes the microbial community of diluvial sand (DS) soil. Further, we assessed the potential of CSS to increase the persistence of human pathogens in DS soil and the colonization of Chinese cabbage (Brassica rapa L. subsp. pekinensis (Lour.) Hanelt). The results revealed that CSS substantially altered the prokaryotic community composition. Moreover, addition of CSS increased the persistence of Salmonella enterica serovar Typhimurium strain 14028s and S. enterica serovar Senftenberg in DS soil. However, the enhanced persistence in soil had no impact on the colonization rate of B. rapa grown on soil inoculated with Salmonella. We detected Salmonella in leaves of 1.9% to 3.6% of plants. Addition of CSS had no impact on the plant colonization rate. The use of sewage sludge composts is an interesting option. However, safety measures should be applied in order to avoid contamination of crop plants by human pathogens. Full article
(This article belongs to the Special Issue Human Pathogens in Primary Production Systems)
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21 pages, 3762 KiB  
Article
Salmonella Heterogeneously Expresses Flagellin during Colonization of Plants
by Azhar A. Zarkani, Nieves López-Pagán, Maja Grimm, María Antonia Sánchez-Romero, Javier Ruiz-Albert, Carmen R. Beuzón and Adam Schikora
Microorganisms 2020, 8(6), 815; https://doi.org/10.3390/microorganisms8060815 - 29 May 2020
Cited by 17 | Viewed by 3331
Abstract
Minimally processed or fresh fruits and vegetables are unfortunately linked to an increasing number of food-borne diseases, such as salmonellosis. One of the relevant virulence factors during the initial phases of the infection process is the bacterial flagellum. Although its function is well [...] Read more.
Minimally processed or fresh fruits and vegetables are unfortunately linked to an increasing number of food-borne diseases, such as salmonellosis. One of the relevant virulence factors during the initial phases of the infection process is the bacterial flagellum. Although its function is well studied in animal systems, contradictory results have been published regarding its role during plant colonization. In this study, we tested the hypothesis that Salmonella’s flagellin plays a versatile function during the colonization of tomato plants. We have assessed the persistence in plant tissues of a Salmonella enterica wild type strain, and of a strain lacking the two flagellins, FljB and FliC. We detected no differences between these strains concerning their respective abilities to reach distal, non-inoculated parts of the plant. Analysis of flagellin expression inside the plant, at both the population and single cell levels, shows that the majority of bacteria down-regulate flagellin production, however, a small fraction of the population continues to express flagellin at a very high level inside the plant. This heterogeneous expression of flagellin might be an adaptive strategy to the plant environment. In summary, our study provides new insights on Salmonella adaption to the plant environment through the regulation of flagellin expression. Full article
(This article belongs to the Special Issue Human Pathogens in Primary Production Systems)
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Review

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18 pages, 1183 KiB  
Review
Plant Bioactive Compounds as an Intrinsic and Sustainable Tool to Enhance the Microbial Safety of Crops
by Andree S. George and Maria T. Brandl
Microorganisms 2021, 9(12), 2485; https://doi.org/10.3390/microorganisms9122485 - 30 Nov 2021
Cited by 15 | Viewed by 3437
Abstract
Outbreaks of produce-associated foodborne illness continue to pose a threat to human health worldwide. New approaches are necessary to improve produce safety. Plant innate immunity has potential as a host-based strategy for the deactivation of enteric pathogens. In response to various biotic and [...] Read more.
Outbreaks of produce-associated foodborne illness continue to pose a threat to human health worldwide. New approaches are necessary to improve produce safety. Plant innate immunity has potential as a host-based strategy for the deactivation of enteric pathogens. In response to various biotic and abiotic threats, plants mount defense responses that are governed by signaling pathways. Once activated, these result in the release of reactive oxygen and nitrogen species in addition to secondary metabolites that aim at tempering microbial infection and pest attack. These phytochemicals have been investigated as alternatives to chemical sanitization, as many are effective antimicrobial compounds in vitro. Their antagonistic activity toward enteric pathogens may also provide an intrinsic hurdle to their viability and multiplication in planta. Plants can detect and mount basal defenses against enteric pathogens. Evidence supports the role of plant bioactive compounds in the physiology of Salmonella enterica, Escherichia coli, and Listeria monocytogenes as well as their fitness on plants. Here, we review the current state of knowledge of the effect of phytochemicals on enteric pathogens and their colonization of plants. Further understanding of the interplay between foodborne pathogens and the chemical environment on/in host plants may have lasting impacts on crop management for enhanced microbial safety through translational applications in plant breeding, editing technologies, and defense priming. Full article
(This article belongs to the Special Issue Human Pathogens in Primary Production Systems)
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