Does the natural life cycle matter for infection?

Does the natural life cycle matter for infection?

Given the over 700 species treated in the Atlas of Clinical Fungi, it is sometimes claimed that almost any fungus can cause a human infection, particularly when the immunity is severely impaired. There is some truth in this idea. Even our friend food fermentation Saccharomyces cerevisiae, or the obligate plant-pathogen Dichotomophthora portulacae causing black stem rot oof purslane can be found in the Atlas. But such infections are ultra-rare; their frequency on the human host compared to that in their natural habitat is close to zero. Even severely compromised patients almost exclusively have a relatively limited spectrum of infections. Newly described infectious agents are mostly recognized by technical advance in diagnostics. Existing fungal species in the environment are in the millions, while the medically relevant species still are only in the hundreds.

The clinical fungi thus must be quite special. Large differences between species are known in natural life cycle, feeding and transmission. Fungi are heterotrophic, living on the degradation of organic matter. Most of these materials concern dead or living vegetation, but few fungi have the ability to degrade materials of plant- as well as animal-origin. A good example is our prime hospital bug, Aspergillus fumigatus, which is also a prevalent compost fungus. Accessible, eroded parts of the human host can be considered as part of its natural habitat, apparently it feels happy on rotting plants as well as in damaged human lungs. This fungus is the optimal example of an opportunist; the animal is part of its natural habitat (Fig. A). Many more fungi are saprobes on dead material, are plant pathogens, or otherwise, having a niche that has nothing to do with animal proteins and therefore are seen in humans only very rarely. In analogy, their relation to the vertebrate host is illustrated in Fig. B. Since their presence in an animal is so exceptional, these fungi cannot be regarded as opportunists.

For real pathogens, the animal host is part of their natural life cycle. They can be transmitted from host to host, as in dermatophytes; then we call them zoophilic pathogens (Fig. C); this category also refers to humans, where in case of adaptation the term anthropophilic pathogens in used. Infections by such fungi are thus contagious. Alternatively, the fungus returns to the environment after infection, to complete its sexual cycle. A subsequent host is then infected via environmental propagules. Such fungi have a double life cycle, and are called environmental pathogens (Fig. D). The main group with this behaviour are the dimorphic pathogens, comprising genera Blastomyces, Histoplasma and relatives. Although they can live happily in the environment, they have an advantage when using an animal vector of transmission and dispersion.

Some fungi cause multiple infections within a short period. The genus Sporothrix provides some famous for causing large epidemics (Zhang et al. 2015), such as the classical outbreak of S. schenckii among South African miners (Helm & Berman 1947) or the South American epidemics by S. brasiliense today (Etchecopaz et al. 2021). In Sporothrix we witness a remarkable change from plant-borne epidemics (Sporothrix globosa; Li et al. 2011) to animal-borne epidemics (S. brasiliensis; Ortiz Sanchotene et al. 2015). The former type of epidemics, originating from a common source of plant material, we call a sapronosis (Fig. E), while when transmitted by cats, as in S. brasiliensis, we speak of a zoonosis (Fig. F). Human Sporothrix infections are not transmitted to a subsequent host, indicating that Homo sapiens is not the preferred host for the fungus. This is different in the zoonoses caused by the zoophilic dermatophyte Microsporum canis (Bassyouni et al. 2017). This fungus can be transmitted, for example, among schoolchildren, but eventually also such an epidemic will die out (Fig. G). Continued human-to-human transmission is seen among anthropophilic dermatophytes (Fig. H), where this host is the preferred habitat of the fungus. Hosts are contagious, and this type of expansion forms a typical epidemic. The recent emergence of Trichophyton indotineae (Kupsch et al. 2019, published under different names) is an example.

The theme above and related questions are discussed in the chapter ‘Natural ecology’ in the Atlas of Clinical Fungi (p. 25 of the print version).

References:

  • Bassyouni RH, El-Sherbiny NA, Abd El Raheem TA & Mohammed BH. 2017. Changing in the epidemiology of tinea capitis among school children in Egypt. Annls Dermatol 29: 13-19.
  • Etchecopaz A, Toscanini MA, Gisbert A, et al. 2021. Sporothrix brasiliensis: a review of an emerging South American fungal pathogen, its related disease, presentation and spread in Argentina. J Fungi (Basel). 7(3): 170.
  • Kupsch C, Czaika VA, Deutsch C, Gräser Y. 2019. Trichophyton mentagrophytes – a new genotype of zoophilic dermatophyte causes sexually transmitted infections. J Deutsch Dermatol Ges 17: 493-501.
  • Helm M, Berman C. 1947. The clinical, therapeutic and epidemiological features of the sporotrichosis infection on the mines. Mine Medical Officers’ Assoc, December 1944, p. 59–67.
  • Li SS, Liu HS, Zheng H, et al. 2011. Clinical analysis of 585 cases of cutaneous sporotrichosis. Chin J Dermatol 44: 161–164 (in Chinese),
  • Ortiz Sanchotene, K., Martins Madrid, I., Baracy Klafke, G., Bergamashi, M., Della Terra, P.P., Rodrigues, A.M., de Camargo, Z.P. & Orzechowski Xavier, M. 2015. Sporothrix brasiliensis outbreaks and the rapid emergence of feline sporotrichosis. Mycoses 58, 652-658
  • Zhang Y, Hagen F, Stielow, B. et al. 2015. Phylogeographic and evolutionary patterns in Sporothrix spanning more than 14 000 human and animal case reports. Persoonia 35: 1-20.