|Plant Signaling & Behaviour: 2007 Nov-Dec; 2(6): 503-504|
The Potential Anti-Herbivory Role of Microorganisms on Plant Thorns
1Department of Biology; Faculty of Science and Science Education; University of Haifa—Oranim; Tivon, Israel
2Department of Evolutionary and Environmental Biology; Faculty of Science and Science Education; University of Haifa—Mount Carmel; Haifa, Israel
Corresponding author.Correspondence to: Malka Halpern; Department of Biology; University of Haifa—Oranim; Tivon 36006 Israel; Tel.: +97.24.983.8978; Fax: +97.24.983.8911; Email: firstname.lastname@example.org
______________________________________________Copyright © 2007 Landes Bioscience
Thorns, spines and prickles are some of the anti-herbivore defenses that plants have evolved. They were recently found to be commonly aposematic (warning coloration). However, the physical anti-herbivore defense executed by these sharp structures seems to be only the tip of the iceberg. We show that thorns of various plant species commonly harbor an array of aerobic and anaerobic pathogenic bacteria including Clostridium perfringens the causative agent of the life-threatening gas gangrene, Bacillus anthracis, and Pantoea agglomerans. Septic inflammation caused by plant thorn injury can result not only from bacteria. Medical literature indicates that thorns, spines or prickles also introduce pathogenic fungi into animals or humans. Dermatophytes that cause subcutaneous mycoses are unable to penetrate the skin and must be introduced into the subcutaneous tissue by a puncture wound. The common microorganism-thorn combinations seem to have been an important contributor to the fact that so many plant thorns are aposematically colored, as a case of convergent evolution of aposematism in these organisms.
Key Words: aposematism, herbivory, pathogen, spine, thorn, bacillus anthracis, clostridium perfringens, sporotrichosis, Mycetoma, subcutaneous mycotic disease
Bacteria and Thorns
Thorns, spines and prickles are a common anti-herbivory mechanical defense in thousands of plant species, especially in arid regions.1,2 The unpalatability of thorny plants is associated with aposematism (warning coloration) in thousands of species.3,4 We proposed that the mechanical protection provided by thorns against large herbivores might not be the whole defensive story. By wounding, thorns may introduce bacteria or fungi into herbivores and cause them severe infections that may be much more dangerous and painful than the thorn's physical injury itself. In a recent publication we showed that thorns from Phoenix dactylifera (date palm) and Crataegus aronia (common hawthorn) harbor an array of pathogenic bacteria.5 The bacteria described and other pathogenic organisms including additional bacteria and fungi that inhabit thorns are most likely involved in both deterring and damaging herbivores, and thus may have uniquely contributed to the common evolution of aposematism in thorny plants as an honest defensive signal.
Pathogenic Bacteria that We Isolated from Thorns
Thorns from several date palm and common hawthorn trees were sampled in the Jordan Valley and Mount Carmel in northern Israel respectively. Every typical mature individual of the two tree species carries thousands of conspicuous aposematic thorns. Although we sampled only a small fraction of thorns found on each tree, we were able to isolate and identify various pathogenic bacterial species from these thorns, which proved it to be a common phenomenon. Fifty-eight bacterial isolates were selected in both aerobic and anaerobic growth conditions, and identified by means of 16S rRNA gene analysis. The isolates belonged to 22 different bacterial species of which 13 are known to be pathogenic to animals or humans: Clostridium perfringens, C. sordellii, C. sardiniens, Bacillus anthracis, B. cereus, B. thuringiensis, B. licheniformis, B. megaterium, Enterococcus faecalis, E. faecium, Rahnella aquatilis, Shigella boydii, and Pantoea agglomerans.5 In an unpublished study, thorns from five individuals, from two thorny shrub species, Sarcopoterium spinosum (thorny burnet) and Alhagi graecorum (manna tree), were also sampled on Mount Carmel. Twenty-seven bacterial isolates that belonged to ten different bacterial species were selected and identified in both aerobic and anaerobic growth conditions. Of these, seven species are known to be pathogenic to animals or humans: Bacillus anthracis, B. cereus, B. thuringiensis, B. licheniformis, B. megaterium, B. circulans, B. pumilus (unpublished data). Pathogenic Bacillus species was found in thorns of trees and shrubs alike.
Micro-organisms can grow on plant surfaces in biofilms (assemblages of bacterial cells attached to a surface and enclosed in adhesive polysaccharides excreted by the cells). Within the biofilm matrix, several different microenvironments can exist, including anoxic conditions. These facilitate the existence of anaerobic bacteria in this specific micro-habitat. Clostridium species isolated and identified from the thorns of date palm and common hawthorn are Gram positive, endospore-forming obligate anaerobic bacteria that cause infections that are associated with wounds. Clostridium perfringens is known to be a flesh-eater since it can produce a necrotizing infection of the skeletal muscle called gas gangrene.6 Clostridium sordellii and C. sardiniense are considered C. perfringens-like strains and were isolated from infected tissues in cases of gas gangrene.7,8 Another species of Clostridium is C. tetani, the etiological agent of tetanus, a serious disease in humans and animals that when untreated can be fatal. Thorn injury was reported in the medical literature to be the cause of tetanus in the USA (from rose bush prickles), Ethiopia and Turkey.9–11
Thorns from three of the sampled plant species (except for thorny burnet) were found to be the habitat for B. anthracis, B. cereus and B. thuringiensis. Bacillus anthracis is the etiological agent of anthrax, a notorious acute fatal disease in animals (domesticated and wild, particularly herbivorous) and humans.12 The cutaneous form of the disease is usually acquired through injured skin or mucous membranes, a typical thorn injury.
The published literature reviewed in Halpern et al.5 has indications from medical case reports that injuries from the plant thorns can result in septic inflammation. Pantoea agglomerans, which in our study was isolated from date palm thorns, has been reported in the medical literature as the cause of septic arthritis after palm thorn injury13 as well as the cause of osteomyelitis and peritonitis after rose prickle injury or unidentified plant thorn injury.14–16
Pathogenic Fungi and Thorns
Septic inflammation caused by plant thorn injury can result not only from bacteria. There are strong indications in the medical literature that thorns, spines or prickles can introduce pathogenic fungi into animals or humans. Dermatophytes that cause subcutaneous mycoses are unable to penetrate the skin. They must be introduced into the subcutaneous tissue by a puncture wound.17 One type of subcutaneous mycosis is chromoblastomycosis, caused by pigmented or dematiaceous saprophytic molds. The most common etiologic agents are Fonsecaea pedrosoi and Cladophialophora carrionii, both of which can be isolated from plants. Infection is acquired by inoculation of the etiologic agent into the subcutaneous tissues of the subject by penetrating thorns or spines of diverse plants.18 Salgado et al.19 reported the isolation of Fonsecaea pedrosoi from thorns of the plant Mimosa pudica at the place of infection identified by one of their patients. Another subcutaneous mycosis is sporotrichosis, caused by the fungus Sporothrix schenckii. This disease occurs throughout the world and is the most common subcutaneous mycotic disease in the USA. The disease is an occupational hazard for florists, gardeners and forestry workers; it is also known as the rose-gardener's disease as it is commonly transmitted by a prick from rose prickles.17,20–22 Mycetoma is a chronic, specific, granulomatous, progressive subcutaneous inflammatory disease with a worldwide geographical distribution. Abscesses in the skin can spread to the bones and muscles. The disease is caused by true fungi or by filamentous bacteria and hence it is classified into Eumycetoma and Actinomycetoma respectively.23 These fungi or bacteria gain access to the tissues via wooden splinters or thorns.23,24
We suggest that thorns, spines and prickles, by wounding, insert pathogenic bacteria or fungi (microorganisms) into the body of herbivores. The injury enables the microorganisms to pass the animal's first and major line of defense (the skin) and cause a disease. Aposematic coloration of thorny plants is common.3,4,25–30 Microorganisms harbored by thorns or spines in plants seem to have enhanced this common, convergent evolution of aposematism in thorny plants, probably because the warning defensive signal is trustworthy.
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