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Agricultural ecosystems are composed of genetically depauperate populations of crop plants grown at a high density and over large spatial scales, with the regional composition of crop species changing little from year to year. These environments are highly conducive for the emergence and dissemination of pathogens. The uniform host populations facilitate the specialization of pathogens to particular crop cultivars and allow the build-up of large population sizes. Population genetic and genomic studies have shed light on the evolutionary mechanisms underlying speciation processes, adaptive evolution and long-distance dispersal of highly damaging pathogens in agro-ecosystems. These studies document the speed with which pathogens evolve to overcome crop resistance genes and pesticides. They also show that crop pathogens can be disseminated very quickly across and among continents through human activities. In this review, we discuss how the peculiar architecture of agro-ecosystems facilitates pathogen emergence, evolution and dispersal. We present four example pathosystems that illustrate both pathogen specialization and pathogen speciation, including different time frames for emergence and different mechanisms underlying the emergence process. Lastly, we argue for a re-design of agro-ecosystems that embraces the concept of dynamic diversity to improve their resilience to pathogens. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

Pathogen emergence is a complex phenomenon that, despite its public health relevance, remains poorly understood. Vibrio vulnificus, an emergent human pathogen, can cause a deadly septicaemia with over 50% mortality rate. To date, the ecological drivers that lead to the emergence of clinical strains and the unique genetic traits that allow these clones to colonize the human host remain mostly unknown. We recently surveyed a large estuary in eastern Florida, where outbreaks of the disease frequently occur, and found endemic populations of the bacterium. We established two sampling sites and observed strong correlations between location and pathogenic potential. One site is significantly enriched with strains that belong to one phylogenomic cluster (C1) in which the majority of clinical strains belong. Interestingly, strains isolated from this site exhibit phenotypic traits associated with clinical outcomes, whereas strains from the second site belong to a cluster that rarely causes disease in humans (C2). Analyses of C1 genomes indicate unique genetic markers in the form of clinical-associated alleles with a potential role in virulence. Finally, metagenomic and physicochemical analyses of the sampling sites indicate that this marked cluster distribution and genetic traits are strongly associated with distinct biotic and abiotic factors (e.g., salinity, nutrients, or biodiversity), revealing how ecosystems generate selective pressures that facilitate the emergence of specific strains with pathogenic potential in a population. This knowledge can be applied to assess the risk of pathogen emergence from environmental sources and integrated toward the development of novel strategies for the prevention of future outbreaks.

We reviewed scientific literature and CABI distribution records published in 2023 to find major plant disease outbreaks and first reports of pathogens spreading in new locations or infecting new host species. This is the third in a series of studies, building on work analysing and documenting reports from 2021 and 2022. We also perform additional analyses to identify time lags between first reports of a disease in a given location and subsequent outbreaks. Pathogens with at least eight articles in the 2023 scientific literature were Xylella fastidiosa, Puccinia striiformis f. sp. tritici, Bursaphelenchus xylophilus, Candidatus Liberibacter asiaticus, Fusarium head blight pathogens (F. graminearum and F. culmorum, which we treated as a single entity), Puccinia graminis f. sp. tritici, Phytophthora infestans, cassava brown streak viruses (cassava brown streak virus and Uganda brown streak virus, which we again treated as one) and tomato leaf curl New Delhi viruses. CABI distribution data from 2023 confirmed new reports for 38 pathogens from 88 records. Pathogens with four or more reports were Meloidogyne enterolobii, Pectobacterium brasiliense, tomato brown rugose fruit virus, Colletotrichum liriopes, Khuskia oryzae, Colletotrichum truncatum, tomato fruit blotch virus, Erysiphe corylacearum, Pantoea ananatis and Ralstonia pseudosolanacearum. As previously, there was little overlap between pathogens identified by reviewing scientific literature versus CABI distribution records. However, the set of pathogens reported in the scientific literature was relatively consistent from 2022 to 2023. Considering reports of outbreaks in the scientific literature from 2020 to 2024, we identify wide variation in intervals between the first report of that pathogen in a country and subsequent disease outbreaks. In some cases, the first report was made over a century ago (for Phytophthora infestans in Ecuador, Xylella fastidiosa in California and Fusarium spp. (pokkah boeng) in China) with major outbreaks still occurring. For other outbreaks, less than a decade had passed since the first report, including Sri Lankan cassava mosaic in Thailand, and Fusarium oxysporum f. sp. cubense in Brazil. We discuss possible reasons for – and implications of – this wide variability in intervals between first report and epidemic emergence.

Erwinia tracheiphila is a virulent phytopathogen that infects two genera of cucurbit crop plants, Cucurbita spp. (pumpkin and squash) and Cucumis spp. (muskmelon and cucumber). One of the unusual ecological traits of this pathogen is that it is limited to temperate eastern North America. Here, we complete the first large-scale sequencing of an E. tracheiphila isolate collection. From phylogenomic, comparative genomic, and empirical analyses, we find that introduced Cucumis spp. crop plants are driving the diversification of E. tracheiphila into multiple lineages. Together, the results from this study show that locally unique biotic (plant population) and abiotic (climate) conditions can drive the evolutionary trajectories of locally endemic pathogens in unexpected ways. Erwinia tracheiphila is the causal agent of bacterial wilt of cucurbits, an economically important phytopathogen affecting few cultivated Cucurbitaceae host plant species in temperate eastern North America. However, essentially nothing is known about E. tracheiphila population structure or genetic diversity. To address this shortcoming, a representative collection of 88 E. tracheiphila isolates was gathered from throughout its geographic range, and their genomes were sequenced. Phylogenomic analysis revealed three genetic clusters with distinct hrp T3SS virulence gene repertoires, host plant association patterns, and geographic distributions. Low genetic heterogeneity within each cluster suggests a recent population bottleneck followed by population expansion. We showed that in the field and greenhouse, cucumber ( Cucumis sativus ), which was introduced to North America by early Spanish conquistadors, is the most susceptible host plant species and the only species susceptible to isolates from all three lineages. The establishment of large agricultural populations of highly susceptible C. sativus in temperate eastern North America may have facilitated the original emergence of E. tracheiphila into cucurbit agroecosystems, and this introduced plant species may now be acting as a highly susceptible reservoir host. Our findings have broad implications for agricultural sustainability by drawing attention to how worldwide crop plant movement, agricultural intensification, and locally unique environments may affect the emergence, evolution, and epidemic persistence of virulent microbial pathogens. IMPORTANCE Erwinia tracheiphila is a virulent phytopathogen that infects two genera of cucurbit crop plants, Cucurbita spp. (pumpkin and squash) and Cucumis spp. (muskmelon and cucumber). One of the unusual ecological traits of this pathogen is that it is limited to temperate eastern North America. Here, we complete the first large-scale sequencing of an E. tracheiphila isolate collection. From phylogenomic, comparative genomic, and empirical analyses, we find that introduced Cucumis spp. crop plants are driving the diversification of E. tracheiphila into multiple lineages. Together, the results from this study show that locally unique biotic (plant population) and abiotic (climate) conditions can drive the evolutionary trajectories of locally endemic pathogens in unexpected ways.

Bivalve molluscan shellfish have been consumed for centuries. Being filter feeders, they may bioaccumulate some microorganisms present in coastal water, either naturally or through the discharge of human or animal sewage. Despite regulations set up to avoid microbiological contamination in shellfish, human outbreaks still occur. After providing an overview showing their implication in disease, this review aims to highlight the diversity of the bacteria or enteric viruses detected in shellfish species, including emerging pathogens. After a critical discussion of the available methods and their limitations, we address the interest of technological developments using genomics to anticipate the emergence of pathogens. In the coming years, further research needs to be performed and methods need to be developed in order to design the future of surveillance and to help risk assessment studies, with the ultimate objective of protecting consumers and enhancing the microbial safety of bivalve molluscan shellfish as a healthy food.

The evolutionary emergence of new pathogens via mutation poses a considerable risk to human and animal populations. Most previous studies have investigated cases where a potentially pandemic strain emerges though mutation from an initial maladapted strain (i.e., its basic reproductive ratioR 0< 1). However, an alternative (and arguably more likely) cause of novel pathogen emergence is where a “weakly adapted” strain (withR 0≈ 1) mutates into a strongly adapted strain (withR 0≫ 1). In this case, a proportion of the host susceptible population is removed as the first strain spreads, but the impact this feedback has on emergence of mutated strains has yet to be quantified. We produce a model of pathogen emergence that takes into account changes in the susceptible population over time and find that the ongoing depletion of susceptible individuals by the first strain has a drastic effect on the emergence probability of the mutated strain, above that assumed by just scaling the reproductive ratio. Finally, we apply our model to the documented emergence of Chikungunya virus on La Réunion Island and demonstrate that the emergence probability of the mutated strain was reduced approximately 10-fold, compared to models assuming that susceptible depletion would not affect outbreak probability. These results highlight the importance of taking population feedbacks into account when predicting disease emergence.

Land use influences disease emergence by changing the ecological dynamics of humans, wildlife, domestic animals, and pathogens. This is a central tenet of One Health, and one that is gaining momentum in wildlife management decision-making in the United States. Using almost 2000 serological samples collected from non-native wild pigs (Sus scrofa) throughout Florida (U.S.), we compared the prevalence and exposure risk of two directly transmitted pathogens, pseudorabies virus (PrV) and Brucella spp., to test the hypothesis that disease emergence would be positively correlated with one of the most basic wildlife management operations: Hunting. The seroprevalence of PrV-Brucella spp. coinfection or PrV alone was higher for wild pigs in land management areas that allowed hunting with dogs than in areas that culled animals using other harvest methods. This pattern did not hold for Brucella alone. The likelihood of exposure to PrV, but not Brucella spp., was also significantly higher among wild pigs at hunted sites than at sites where animals were culled. By failing to consider the impact of dog hunting on the emergence of non-native pathogens, current animal management practices have the potential to affect public health, the commercial livestock industry, and wildlife conservation.

Pathogenicity and genetic diversity of Fusarium oxysporum from geographically widespread native Gossypium populations, including a cotton growing area believed to be the center of origin of VCG 01111 and VCG 01112 of F. oxysporum f. sp. vasinfectum (Fov) in Australia, was determined using glasshouse bioassays and AFLPs. Five lineages (A–E) were identified among 856 isolates. Of these, 12% were strongly pathogenic on cotton, 10% were weakly pathogenic and designated wild Fov, while 78% were nonpathogenic. In contrast to the occurrence of pathogenic isolates in all five lineages in soils associated with wild Gossypium, in cotton growing areas only three lineages (A, B, E) occurred and all pathogenic isolates belonged to two subgroups in lineage A. One of these contained VCG 01111 isolates while the other contained VCG 01112 isolates. Sequence analyses of translation elongation factor‐1α, mitochondrial small subunit rDNA, nitrate reductase and phosphate permease confirmed that Australian Fov isolates were more closely related to lineage A isolates of native F. oxysporum than to Fov races 1–8 found overseas. These results strongly support a local evolutionary origin for Fov in Australian cotton growing regions.

In recent years, the number of emergent plant pathogens (EPPs) has grown substantially, threatening agroecosystem stability and native biodiversity. Contributing factors include, among others, shifts in biogeography, with EPP spread facilitated by the global unification of monocultures in modern agriculture, high volumes of trade in plants and plant products and an increase in sexual recombination within pathogen populations. The unpredictable nature of EPPs as they move into new territories is a situation that has led to sudden and widespread epidemics. Understanding the underlying causes of pathogen emergence is key to managing the impact of EPPs. Here, we review some factors specifically influencing the emergence of oomycete and fungal EPPs, including new introductions through anthropogenic movement, natural dispersal and weather events, as well as genetic factors linked to shifts in host range.