Penicillium

Last updated

Penicillium
Penicillium Pengo.jpg
Penicillium sp.
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Eurotiomycetes
Order: Eurotiales
Family: Aspergillaceae
Genus: Penicillium
Link (1809)
Type species
Penicillium expansum
Link (1809)
Species

over 300

Synonyms [1]
List
  • AspergillopsisSopp (1912)
  • CarpentelesLangeron (1922)
  • ChromocleistaYaguchi & Udagawa (1993)
  • CitromycesWehmer (1893)
  • CoremiumLink (1809)
  • EladiaG. Sm. (1961)
  • EupenicilliumF. Ludw. (1892)
  • Floccaria Grev. (1827)
  • HemicarpentelesA. K. Sarbhoy & Elphick (1968)
  • MoniligerLetell. (1839)
  • Pritzeliella Henn. (1903)
  • ThysanophoraW.B. Kendr. (1961)
  • ToluromycesDelitsch (1943)
  • Walzia Sorokin (1871)

Penicillium ( /ˌpɛnɪˈsɪliəm/ ) is a genus of ascomycetous fungi that is part of the mycobiome of many species and is of major importance in the natural environment, in food spoilage, and in food and drug production.

Contents

Some members of the genus produce penicillin, a molecule that is used as an antibiotic, which kills or stops the growth of certain kinds of bacteria. Other species are used in cheesemaking. According to the Dictionary of the Fungi (10th edition, 2008), the widespread genus contains over 300 species. [2]

Taxonomy

The genus was first described in the scientific literature by Johann Heinrich Friedrich Link in his 1809 work Observationes in ordines plantarum naturales; he wrote, "Penicillium. Thallus e floccis caespitosis septatis simplicibus aut ramosis fertilibus erectis apice penicillatis", where penicillatis means "having tufts of fine hair". [3] [4] Link included three species— P. candidum , P. expansum , and P. glaucum —all of which produced a brush-like conidiophore (asexual spore-producing structure). The common apple rot fungus P. expansum was later selected as the type species. [5]

In his 1979 monograph, John I. Pitt divided Penicillium into four subgenera based on conidiophore morphology and branching pattern: Aspergilloides, Biverticillium, Furcatum, and Penicillium. [6] Species included in subgenus Biverticillium were later merged into Talaromyces .

Species

Various fungi including Penicillium and Aspergillus species growing in axenic culture Ascomycetes.jpg
Various fungi including Penicillium and Aspergillus species growing in axenic culture
Some penicillium mold on mandarin oranges, probably Penicillium digitatum. Penicilliummandarijntjes.jpg
Some penicillium mold on mandarin oranges, probably Penicillium digitatum.

Selected species include;

Etymology

The genus name is derived from the Latin root penicillum, meaning "painter's brush", and refers to the chains of conidia that resemble a broom. [7]

Characteristics

Penicillium sp. under bright field microscopy (10 x 100 magnification) with lactophenol cotton blue stain Penicillium Spp..jpg
Penicillium sp. under bright field microscopy (10 × 100 magnification) with lactophenol cotton blue stain

The thallus (mycelium) consists of highly branched networks of multinucleated, usually colourless hyphae, with each pair of cells separated by a septum. Conidiophores are at the end of each branch accompanied by green spherical constricted units called conidia. These propagules play a significant role in reproduction; conidia are the main dispersal strategy of these fungi. [8]

Sexual reproduction involves the production of ascospores, commencing with the fusion of an archegonium and an antheridium, with sharing of nuclei. The irregularly distributed asci contain eight unicellular ascospores each.

Ecology

Species of Penicillium are ubiquitous soil fungi preferring cool and moderate climates, commonly present wherever organic material is available. Saprophytic species of Penicillium and Aspergillus are among the best-known representatives of the Eurotiales and live mainly on organic biodegradable substances. Commonly known in America as molds, they are among the main causes of food spoilage, especially species of subgenus Penicillium. [9] Many species produce highly toxic mycotoxins. The ability of these Penicillium species to grow on seeds and other stored foods depends on their propensity to thrive in low humidity and to colonize rapidly by aerial dispersion while the seeds are sufficiently moist. [10] Some species have a blue color, commonly growing on old bread and giving it a blue fuzzy texture.

Some Penicillium species affect the fruits and bulbs of plants, including P. expansum , apples and pears; P. digitatum , citrus fruits; [11] and P. allii , garlic. [12] Some species are known to be pathogenic to animals; P. corylophilum , P. fellutanum , P. implicatum , P. janthinellum , P. viridicatum , and P. waksmanii are potential pathogens of mosquitoes. [13]

Penicillium species are present in the air and dust of indoor environments, such as homes and public buildings. The fungus can be readily transported from the outdoors, and grow indoors using building material or accumulated soil to obtain nutrients for growth. Penicillium growth can still occur indoors even if the relative humidity is low, as long as there is sufficient moisture available on a given surface. A British study determined that Aspergillus- and Penicillium-type spores were the most prevalent in the indoor air of residential properties, and exceeded outdoor levels. [14] Even ceiling tiles can support the growth of Penicillium—as one study demonstrated—if the relative humidity is 85% and the moisture content of the tiles is greater than 2.2%. [15]

Some Penicillium species cause damage to machinery and the combustible materials and lubricants used to run and maintain them. For example, P. chrysogenum (formerly P. notatum), P. steckii ,   P. cyclopium , and P. nalgiovensis affect fuels; P. chrysogenum, P. rubrum , and P. verrucosum cause damage to oils and lubricants; P. regulosum damages optical and protective glass. [16]

Economic value

Penicillin core.svg
Core structure of penicillin
Griseofulvin.svg
Griseofulvin

Several species of the genus Penicillium play a central role in the production of cheese and of various meat products. To be specific, Penicillium molds are found in blue cheese. Penicillium camemberti and Penicillium roqueforti are the molds on Camembert, Brie, Roquefort, and many other cheeses. Penicillium nalgiovense is used in soft mold-ripened cheeses, such as Nalžovy (ellischau) cheese, and to improve the taste of sausages and hams, and to prevent colonization by other molds and bacteria. [17] [18]

In addition to their importance in the food industry, species of Penicillium and Aspergillus serve in the production of a number of biotechnologically produced enzymes and other macromolecules, such as gluconic, citric, and tartaric acids, as well as several pectinases, lipase, amylases, cellulases, and proteases. Some Penicillium species have shown potential for use in bioremediation, more specifically mycoremediation, because of their ability to break down a variety of xenobiotic compounds. [19]

The genus includes a wide variety of species molds that are the source molds of major antibiotics. Penicillin, a drug produced by P. chrysogenum (formerly P. notatum), was accidentally discovered by Alexander Fleming in 1929, and found to inhibit the growth of Gram-positive bacteria (see beta-lactams). Its potential as an antibiotic was realized in the late 1930s, and Howard Florey and Ernst Chain purified and concentrated the compound. The drug's success in saving soldiers in World War II who had been dying from infected wounds resulted in Fleming, Florey and Chain jointly winning the Nobel Prize in Medicine in 1945. [20]

Griseofulvin is an antifungal drug and a potential chemotherapeutic agent [21] that was discovered in P. griseofulvum . [22] Additional species that produce compounds capable of inhibiting the growth of tumor cells in vitro include: P. pinophilum , [23] P. canescens , [24] and P. glabrum . [24]

Reproduction

Although many eukaryotes are able to reproduce sexually, as much as 20% of fungal species had been thought to reproduce exclusively by asexual means. However recent studies have revealed that sex occurs even in some of the supposedly asexual species. For example, sexual capability was recently shown for the fungus Penicillium roqueforti , used as a starter for blue cheese production. [25] This finding was based, in part, on evidence for functional mating type (MAT) genes that are involved in fungal sexual compatibility, and the presence in the sequenced genome of most of the important genes known to be involved in meiosis. Penicillium chrysogenum is of major medical and historical importance as the original and present-day industrial source of the antibiotic penicillin. The species was considered asexual for more than 100 years despite concerted efforts to induce sexual reproduction. However, in 2013, Bohm et al. [26] finally demonstrated sexual reproduction in P. chrysogenum.

These findings with Penicillium species are consistent with accumulating evidence from studies of other eukaryotic species that sex was likely present in the common ancestor of all eukaryotes. [27] Furthermore, these recent results suggest that sex can be maintained even when very little genetic variability is produced.

Prior to 2013, when the "one fungus, one name" nomenclature change came into effect, Penicillium was used as the genus for anamorph (clonal forms) of fungi and Talaromyces was used for the teleomorph (sexual forms) of fungi. After 2013 however, fungi were reclassified based on their genetic relatedness to each other and now the genera Penicillium and Talaromyces both contain some species capable of only clonal reproduction and others that can reproduce sexually.

Related Research Articles

<span class="mw-page-title-main">Ascomycota</span> Division or phylum of fungi

Ascomycota is a phylum of the kingdom Fungi that, together with the Basidiomycota, forms the subkingdom Dikarya. Its members are commonly known as the sac fungi or ascomycetes. It is the largest phylum of Fungi, with over 64,000 species. The defining feature of this fungal group is the "ascus", a microscopic sexual structure in which nonmotile spores, called ascospores, are formed. However, some species of Ascomycota are asexual and thus do not form asci or ascospores. Familiar examples of sac fungi include morels, truffles, brewers' and bakers' yeast, dead man's fingers, and cup fungi. The fungal symbionts in the majority of lichens such as Cladonia belong to the Ascomycota.

<span class="mw-page-title-main">Mold</span> Wooly, dust-like fungal structure or substance

A mold or mould is one of the structures that certain fungi can form. The dust-like, colored appearance of molds is due to the formation of spores containing fungal secondary metabolites. The spores are the dispersal units of the fungi. Not all fungi form molds. Some fungi form mushrooms; others grow as single cells and are called microfungi.

<i>Talaromyces marneffei</i> Species of fungus

Talaromyces marneffei, formerly called Penicillium marneffei, was identified in 1956. The organism is endemic to southeast Asia where it is an important cause of opportunistic infections in those with HIV/AIDS-related immunodeficiency. Incidence of T. marneffei infections has increased due to a rise in HIV infection rates in the region.

<i>Aspergillus</i> Genus of fungi

Aspergillus is a genus consisting of several hundred mould species found in various climates worldwide.

<i>Penicillium roqueforti</i> Species of fungus

Penicillium roqueforti is a common saprotrophic fungus in the genus Penicillium. Widespread in nature, it can be isolated from soil, decaying organic matter, and plants.

<i>Penicillium camemberti</i> Species of fungus

Penicillium camemberti is a species of fungus in the genus Penicillium. It is used in the production of Camembert, Brie, Langres, Coulommiers, and Cambozola cheeses, on which colonies of P. camemberti form a hard, white crust. It is responsible for giving these cheeses their distinctive flavors. An allergy to the antibiotic penicillin does not necessarily imply an allergy to cheeses made using P. camemberti.

<i>Penicillium expansum</i> Species of fungus

Penicillium expansum is a psychrophilic blue mold that is common throughout the world in soil. It causes Blue Mold of apples, one of the most prevalent and economically damaging post-harvest diseases of apples.

The parasexual cycle, a process restricted to fungi and single-celled organisms, is a nonsexual mechanism of parasexuality for transferring genetic material without meiosis or the development of sexual structures. It was first described by Italian geneticist Guido Pontecorvo in 1956 during studies on Aspergillus nidulans. A parasexual cycle is initiated by the fusion of hyphae (anastomosis) during which nuclei and other cytoplasmic components occupy the same cell. Fusion of the unlike nuclei in the cell of the heterokaryon results in formation of a diploid nucleus (karyogamy), which is believed to be unstable and can produce segregants by recombination involving mitotic crossing-over and haploidization. Mitotic crossing-over can lead to the exchange of genes on chromosomes; while haploidization probably involves mitotic nondisjunctions which randomly reassort the chromosomes and result in the production of aneuploid and haploid cells. Like a sexual cycle, parasexuality gives the species the opportunity to recombine the genome and produce new genotypes in their offspring. Unlike a sexual cycle, the process lacks coordination and is exclusively mitotic.

<span class="mw-page-title-main">Fungus</span> Biological kingdom, separate from plants and animals

A fungus is any member of the group of eukaryotic organisms that includes microorganisms such as yeasts and molds, as well as the more familiar mushrooms. These organisms are classified as one of the traditional eukaryotic kingdoms, along with Animalia, Plantae and either Protista or Protozoa and Chromista.

<i>Penicillium chrysogenum</i> Species of fungus

Penicillium chrysogenum is a species of fungus in the genus Penicillium. It is common in temperate and subtropical regions and can be found on salted food products, but it is mostly found in indoor environments, especially in damp or water-damaged buildings. It has been recognised as a species complex that includes P. notatum, P. meleagrinum, and P. cyaneofulvum. Molecular phylogeny has established that Alexander Fleming's first discovered penicillin producing strain is of a distinct species, P. rubens, and not of P. notatum. It has rarely been reported as a cause of human disease. It is the source of several β-lactam antibiotics, most significantly penicillin. Other secondary metabolites of P. chrysogenum include roquefortine C, meleagrin, chrysogine, 6-MSA YWA1/melanin, andrastatin A, fungisporin, secalonic acids, sorbicillin, and PR-toxin.

<span class="mw-page-title-main">Fungi imperfecti</span> Fungal classification based on asexual characters when sexual reproduction is unidentified

The fungi imperfecti or imperfect fungi are fungi which do not fit into the commonly established taxonomic classifications of fungi that are based on biological species concepts or morphological characteristics of sexual structures because their sexual form of reproduction has never been observed. They are known as imperfect fungi because only their asexual and vegetative phases are known. They have asexual form of reproduction, meaning that these fungi produce their spores asexually, in the process called sporogenesis.

<span class="mw-page-title-main">Charles Thom</span> American icrobiologist and mycologist (1872–1956)

Charles Thom was an American microbiologist and mycologist. Born and raised in Illinois, he received his PhD from the University of Missouri, the first such degree awarded by that institution. He studied the microbiology of dairy products and soil fungi, and in particular researched the genera Aspergillus and Penicillium. His work influenced the establishment of standards for food handling and processing in the USA. He pioneered the use of culture media to grow microorganisms, and, with food chemist James N. Currie, developed a process to mass-produce citric acid using Aspergillus. Thom played an important role in the development of penicillin in World War II.

<i>Penicillium rubens</i> Species of fungus

Penicillium rubens is a species of fungus in the genus Penicillium and was the first species known to produce the antibiotic penicillin. It was first described by Philibert Melchior Joseph Ehi Biourge in 1923. For the discovery of penicillin from this species Alexander Fleming shared the Nobel Prize in Physiology or Medicine in 1945. The original penicillin-producing type has been variously identified as Penicillium rubrum, P. notatum, and P. chrysogenum among others, but genomic comparison and phylogenetic analysis in 2011 resolved that it is P. rubens. It is the best source of penicillins and produces benzylpenicillin (G), phenoxymethylpenicillin (V) and octanoylpenicillin (K). It also produces other important bioactive compounds such as andrastin, chrysogine, fungisporin, roquefortine, and sorbicillins.

Medicinal fungi are fungi that contain metabolites or can be induced to produce metabolites through biotechnology to develop prescription drugs. Compounds successfully developed into drugs or under research include antibiotics, anti-cancer drugs, cholesterol and ergosterol synthesis inhibitors, psychotropic drugs, immunosuppressants and fungicides.

Penicillium carneum is a fungus species of the genus of Penicillium.Penicillium roqueforti var. carneum was reclassified to Penicillium carneum.P. carneum was isolated from spoiled meat products, silage, rye bread, water, beer, cheese, mouldy barkers yeast and cork. P. carneum produces patulin, penicillic acid, penitrem A, mycophenolic acid roquefortines.

Penicillium psychrosexualis is a filamentous fungus in the genus Penicillium. Described as new to science in 2010, the species was found growing on refrigerated moldy apples in the Netherlands. It is closely related to the blue cheese fungus P. roqueforti.

<i>Penicillium digitatum</i> Species of fungus

Penicillium digitatum is a mesophilic fungus found in the soil of citrus-producing areas. It is a major source of post-harvest decay in fruits and is responsible for the widespread post-harvest disease in Citrus fruit known as green rot or green mould. In nature, this necrotrophic wound pathogen grows in filaments and reproduces asexually through the production of conidiophores and conidia. However, P. digitatum can also be cultivated in the laboratory setting. Alongside its pathogenic life cycle, P. digitatum is also involved in other human, animal and plant interactions and is currently being used in the production of immunologically based mycological detection assays for the food industry.

<span class="mw-page-title-main">Human interactions with fungi</span> Overview of human—fungi interactions

Human interactions with fungi include both beneficial uses, whether practical or symbolic, and harmful interactions such as when fungi damage crops, timber, food, or are pathogenic to animals.

Penicillium commune is an indoor fungus belonging to the genus Penicillium. It is known as one of the most common fungi spoilage moulds on cheese. It also grows on and spoils other foods such as meat products and fat-containing products like nuts and margarine. Cyclopiazonic acid and regulovasine A and B are the most important mycotoxins produced by P. commune. The fungus is the only known species to be able to produce both penitrem A and roquefortine. Although this species does not produce penicillin, it has shown to have anti-pathogenic activity. There are no known plant, animal or human diseases caused by P. commune.

Aspergillus giganteus is a species of fungus in the genus Aspergillus that grows as a mold. It was first described in 1901 by Wehmer, and is one of six Aspergillus species from the Clavati section of the subgenus Fumigati. Its closest taxonomic relatives are Aspergillus rhizopodus and Aspergillus longivescia.

References

  1. ↑ Page Penicillium on "Mycobank". Westerdijk Fungal Biodiversity Institute . Retrieved 2023-09-20.
  2. ↑ Kirk, PM; Cannon, PF; Minter, DW; Stalpers, JA (2008). Dictionary of the Fungi (10th ed.). Wallingford, UK: CABI. p.  505. ISBN   978-0-85199-826-8.
  3. ↑ Identification and nomenclature of the genus Penicillium, C.M. Visagie1, J. Houbraken1, , , J.C. Frisvad2, , , S.-B. Hong3, C.H.W. Klaassen4, G. Perrone5, K.A. Seifert6, J. Varga7, T. Yaguchi8, R.A. Samson, 22 September 2014, https://dx.doi.org/10.1016/j.simyco.2014.09.001
  4. ↑ Link, JHF (1809). "Observationes in ordines plantarum naturales. Dissertatio I". Magazin der Gesellschaft Naturforschenden Freunde Berlin (in Latin). 3: 3–42.
  5. ↑ Samson, R.A.; Pitt, J.I. (1985). Advances in Penicillium and Aspergillus Systematics . Springer. ISBN   978-0-306-42222-5.
  6. ↑ Pitt, J.I. (1979). The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic Press. ISBN   978-0-12-557750-2.
  7. ↑ Haubrich, W.S. (2003). Medical Meanings: A Glossary of Word Origins (2nd ed.). Philadelphia, Pennsylvania: American College of Physicians. p. 175. ISBN   978-1-930513-49-5 . Retrieved 2013-02-03.
  8. ↑ Pitt, J. (1985). "A laboratory guide to common Penicillium species". 79: 491. doi:10.2307/3807483. JSTOR   3807483. S2CID   84610634.{{cite journal}}: Cite journal requires |journal= (help)
  9. ↑ Samson RA, Seifert KA, Kuijpers AF, Houbraken JA, Frisvad JC (2004). "Phylogenetic analysis of Penicillium subgenus Pencillium using partial beta-tubulin sequences" (PDF). Studies in Mycology. 49: 175–200. Archived from the original (PDF) on 2012-03-22. Retrieved 2011-07-14.
  10. ↑ Pitt JI, Basílico JC, Abarca ML, López C (2000). "Mycotoxins and toxigenic fungi". Medical Mycology. 38 (Suppl 1): 41–46. doi:10.1080/714030911. PMID   11204163.
  11. ↑ Balgrie, B. (2003). Taints and Off-flavours in Food. CRC Press. p. 134. ISBN   978-1-85573-449-4 . Retrieved 2013-02-03.
  12. ↑ Valdez JG, Makuch MA, Ordovini AF, Masuelli RW, Overy DP, Piccolo RJ (2006). "First report of Penicillium allii as a field pathogen of garlic (Allium sativum)". Plant Pathology. 55 (4): 583. doi: 10.1111/j.1365-3059.2006.01411.x . hdl: 11336/147639 .
  13. ↑ da Costa, GL; de Moraes, AM; de Oliveira, PC (1998). "Pathogenic action of Penicillium species on mosquito vectors of human tropical diseases". Journal of Basic Microbiology. 38 (5–6): 337–41. doi:10.1002/(SICI)1521-4028(199811)38:5/6<337::AID-JOBM337>3.0.CO;2-N. PMID   9871331. S2CID   221867835.
  14. ↑ Fairs, A.; Wardlaw, AJ; Thompson, JR; Pashley, CH (2010). "Guidelines on ambient intramural airborne fungal spores". Journal of Investigational Allergology and Clinical Immunology. 20 (6): 490–98. PMID   21243933.
  15. ↑ Chang, JCS; Foarde, KK; Vanosdell, DW. (1995). "Growth evaluation of fungi (Penicillium and Aspergillus spp.) on ceiling tiles". Atmospheric Environment. 29 (17): 2331 37. Bibcode:1995AtmEn..29.2331C. doi:10.1016/1352-2310(95)00062-4.
  16. ↑ Semenov SA, Gumargalieva KZ, Zaikov GE (2003-08-01). Biodegradation and Durability of Materials Under the Effect of Microorganisms (New Concepts in Polymer Science). V.S.P. Intl Science. pp. 34–35. ISBN   978-90-6764-388-7.
  17. ↑ Mrázek, J; Pachlová, V; Buňka, F; Černíková, M; Dráb, V; Bejblová, M; Staněk, K; Buňková, L (11 September 2015). "Effects of different strains Penicillium nalgiovense in the Nalžovy cheese during ripening". Journal of the Science of Food and Agriculture. 96 (7): 2547–54. doi:10.1002/jsfa.7375. PMID   26251231.
  18. ↑ Marianski, S.; Marianski, A. (2009). The Art of Making Fermented Sausages. Seminole, Florida: Bookmagic. p. 47. ISBN   978-0-9824267-1-5 . Retrieved 2013-02-03.
  19. ↑ Leitão, A.L. (2009). "Potential of Penicillium species in the bioremediation field". International Journal of Environmental Research and Public Health. 6 (4): 1393–417. doi: 10.3390/ijerph6041393 . PMC   2681198 . PMID   19440525.
  20. ↑ Rifkind, D.; Freeman, G. (2005). The Nobel Prize Winning Discoveries in Infectious Diseases. London, UK: Academic Press. pp. 43–46. ISBN   978-0-12-369353-2 . Retrieved 2013-02-03.
  21. ↑ Singh P, Rathinasamy K, Mohan R, Panda D (2008). "Microtubule assembly dynamics: an attractive target for anticancer drugs". IUBMB Life. 60 (6): 368–75. doi: 10.1002/iub.42 . PMID   18384115. S2CID   111334.
  22. ↑ De Carli, L.; Larizza, L. (1988). "Griseofulvin". Mutation Research. 195 (2): 91–126. doi:10.1016/0165-1110(88)90020-6. PMID   3277037.
  23. ↑ Nicoletti R, Manzo E, Ciavatta ML (2009). "Occurrence and bioactivities of funicone-related compounds". International Journal of Molecular Sciences. 10 (4): 1430–44. doi: 10.3390/ijms10041430 . PMC   2680625 . PMID   19468317.
  24. 1 2 Nicoletti, R.; Buommino, E.; De Filippis, A.; Lopez-Gresa, M.; Manzo, E.; Carella, A; Petrazzuolo, M; Tufano, M.A. (2009). "Bioprospecting for antagonistic Penicillium strains as a resource of new antitumor compounds". World Journal of Microbiology and Biotechnology. 24 (2): 185–95. doi:10.1007/s11274-007-9455-y. S2CID   86101370.
  25. ↑ Ropars J, Dupont J, Fontanillas E, Rodríguez de la Vega RC, Malagnac F, Coton M, Giraud T, López-Villavicencio M (2012). "Sex in cheese: evidence for sexuality in the fungus Penicillium roqueforti". PLOS ONE. 7 (11): e49665. Bibcode:2012PLoSO...749665R. doi: 10.1371/journal.pone.0049665 . PMC   3504111 . PMID   23185400.
  26. ↑ Böhm J, Hoff B, O'Gorman CM, Wolfers S, Klix V, Binger D, Zadra I, Kürnsteiner H, Pöggeler S, Dyer PS, Kück U (January 2013). "Sexual reproduction and mating-type-mediated strain development in the penicillin-producing fungus Penicillium chrysogenum". Proc. Natl. Acad. Sci. U.S.A. 110 (4): 1476–81. doi: 10.1073/pnas.1217943110 . PMC   3557024 . PMID   23307807.
  27. ↑ Malik SB, Pightling AW, Stefaniak LM, Schurko AM, Logsdon JM (2008). "An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis". PLOS ONE. 3 (8): e2879. Bibcode:2008PLoSO...3.2879M. doi: 10.1371/journal.pone.0002879 . PMC   2488364 . PMID   18663385.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.