2. Insights into cross-kingdom plant pathogenic bacteria

Life on Earth is diverse and interactive: not one ecosystem harboring a single species has yet been described. Interactions between organisms can be very diverse in nature, ranging from beneficial through neutral to detrimental. An infectious disease is usually defined as the result of a detrimental (set of) interaction(s), and is usually restricted to a given combination of host (the diseased) and pathogen (the disease-causing agent). The infectious disease may be defined as a biological process leading to the disruption of the normal physiology of a multicellular organism in response to the presence of a pathogenic microorganism on or in the body.

 Diseases may differ in their presentation but infections are always preceded by adhesion, invasion and colonization. Interestingly, several pathogenic microorganisms are capable of infecting a variety of organisms, and in some cases even members of different biological kingdoms of life may be susceptible. Such cross-kingdom host jumps are defined when a microorganism normally colonizing a species from one taxonomic kingdom becomes able to repeatedly infect a species belonging to another kingdom. Microbial pathogen host jumps occurring at across-kingdom level are not as well-known as those occurring within the animal kingdom, such as those associated with human diseases, but several cross-kingdom host jumps have been described andhave highlighted the ability of seemingly dedicated human pathogens to cause plant disease, and specialized plant pathogens to cause human disease.

The phrase “human pathogens on plants” (HPOPs) has been proposed recently to describe such pathogens when they inhabit, colonize, enter, or otherwise interact with plants.

The disease strategies used by cross-kingdom pathogens to infect unrelated hosts are of particular interest, since plant and animal (human) hosts have distinctive physical barriers and defense responses. While specialists may have evolved dedicated factors for overcoming the physical barriers and innate defenses in a certain host, a cross-kingdom pathogen would require a diverse library of genes and disease strategies to overcome the specific defense obstacles of each of its hosts. This would either necessitate a suite of pathogenicity factors to enable attachment, disease development, and dispersal for each host, or a universal disease strategy in which the same suite of pathogenicity factors is used for all hosts. Phytopathogens utilize specific determinants that help to breach reinforced cell walls and manipulate plant physiology to facilitate the disease process, while human pathogens use determinants for exploiting mammalian physiology and overcoming highly developed adaptive immune responses.

 Potential cross-kingdom pathogenic microorganisms must be able to come into close and frequent contact with potential hosts, and must be able to overcome or evade host defences. Reproduction on, in, or near the new host will ensure the transmission or release of successful genotypes. Signatures of host adaptation will be apparent in these determinants, which may include incremental mutations and genetic rearrangements, along with the acquisition of novel genetic elements that may contribute to virulence or host specificity. The identification of these genetic determinants in cross-kingdom pathogens with both human- and plant-pathogenic potential can provide a better understanding of the evolution of phytopathogenicity, as well as the role of plants as potential reservoirs for clinically relevant bacteria.

An unexpectedly high number of cross-kingdom host shifts of bacterial and fungal pathogens have been described. The Gram-negative bacterial family Enterobacteriaceae, which includes many human pathogens (e.g., Escherichia, Salmonella, and Shigella) associated with plant foods, also contains a number of genera of plant pathogens (Enterobacter, Erwinia, Pantoea, Pectobacterium, etc.), which cause plant diseases such as blights, wilts, and soft rots. The taxonomic relatedness of these plant and human pathogens raises interesting questions about the possibilities for niche competition or synergism, horizontal nucleic acid exchange in protected plant niches, or even host range expansion.

There are microbial species, sometimes referred to as cross-over pathogens that infect and cause disease on both plants and humans, though these are relatively uncommon. Examples of currently recognized cross-kingdom pathogens include a few bacterial species that commonly inhabit plant surfaces and the rhizosphere, such as Pseudomonas aeruginosa, Burkholderia cepacia, Dickeya spp., Enterococcus faecalis, Serratia marcescens, Agrobacterium tumefaciens, Phytophthora infestans, Salmonella enterica, Escherichiacoli, and Listeria monocytogenes.