Wikipedia

Torula herbarum

Torula herbarum is a darkly-pigmented filamentous fungus in the phylum Ascomycota.[1] It is often included in the unrelated but morphologically similar group of fungi known as sooty molds.[2] It was first described by Persoon in the genus Monilinia based on similarity to the agent of brown rot of stone fruit but later transferred to the genus Torula by Link. Conidia of T. herbarum are dark brown or olivaceous colour and have a distinctive shape and number of cells.[3] T. herbarum produces secondary metabolites with cytotoxic activity towards bacteria and human cancer cells.[4]

Torula herbarum
Scientific classification
Kingdom:
Fungi
Division:
Ascomycota
Subdivision:
Pezizomycotina
Class:
Dothideomycetes
Order:
Pleosporales
Family:
Torulaceae
Genus:
Torula
Species:
T. herbarum
Binomial name
Torula herbarum
(Pers.) Link (1809)
Synonyms
  • Monilia herbarum Pers. (1801)
  • Torula monilis Pers. (Usteri) (1795)
  • Torula herbarum f. quaternella Sacc. (1913)
  • Torula herbarum var. cereicola Speg. (1921)

History and taxonomy

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Torula herbarum was first described by Christiaan Hendrik Persoon under the genus Monilia or Monilinia,[5] in 1801 in Göttingen. In 1809, Johann Heinrich Friedrich Link transferred the fungus to the genus Torula, as T. herbarum. Several forms and variations of T. herbarum have been named, including T. herbarum f. quaternella in 1913 and T. herbarum var. cereicola in 1921.[6]

Growth and morphology

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The genus Torula is defined as dematiaceous[7] hyphomycetes, or more commonly, darkly pigmented fungi that grow slowly and reproduce asexually by conidia in string of beads-like chains.[1] The fungal colonies are variable in size. They can range from 1–2 mm diameter patches to covering large areas and encircling stems.[8] They appear to be olivaceous (musky yellow green) in colour when growing and dark brown when matured. They are discrete, dry[9] and have a felty, fuzzy and velvety appearance.[8]

 
Diagram depicting formation of corona cell in Torula herbarum

The mycelium can be superficial or immersed and hyaline branched,[9][3] relative to the rest of the structure.[6] They are unbranched and usually colourless or a mid-brown colour. They appear to be smooth and 2-6 μm in diameter.[6] Some other reports state they are wider, darker and thicker cells.[8] The conidiophores will become the conidiogenous (promotes conidiogenesis) cells that are 7-9 μm in diameter, monoblastic (single or single-celled) or polyblastic (multiple celled).[9][6] The conidiophores are globose or ellipsoidal (football shape),[9] smooth and slightly bumpy at the fertile end.

In culture, colonies can cover an entire Petri dish of suitable growth medium after 2 weeks of incubation at 25 °C.[9] Colonies are flat, smooth and distributed evenly with moderate aerial mycelium and a distinct edge.[9] The colour is olivaceous-grey on the reverse side and paler on the surface when grown on Potato dextrose agar (PDA) and Malt Extract Agar (MEA) plates.[9][6]

The conidia of T. herbarum are typically 3-5 celled, dark brown or black colour and rough-walled with prickly or spiny ornamentation resembling a burned crust appearance.[10][6] The apical cell is usually more lightly pigmented than the lower cells, and at maturity it tends to collapse inward forming a characteristic structure called a "corona (crown) cell".[1][9] The conidia are dry and form in unbranched or branched chains the break apart readily.[8] with textured walls either like studded elevations or smaller pricks or spines. The chains may have a zig-zag pattern where one branch is more dominant (sympodial growth).[8]

Habitat and ecology

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T. herbarum is a cosmopolitan species that is most commonly found in temperate climate regions,[11] and exists in most areas with a suitable climate, including: Canada, India, United States of America, Cuba, Kenya, India, etc.[6] It thrives on plant debris, on trees and in soil,[11][12] often on or in dead herbaceous stems.[6] It is a rot fungus that creates dark brown lesions sometimes in bands.[6] A blight disease of ber, Ziziphus mauritiana, is caused by T. herbarum.[13] In one study, T. herbarum accounted for 47% of the fungi recovered from earthworm casts and 6% of the mycota from non-earthworm associated soils.[12] Less commonly, it can be found on wood and calcareous and siliceous rocks as well.[6] Accordingly, items made out of those materials such as baskets, wood furniture, paper, tiles, linoleum and concrete may contain spores of this species.[6] In autumn, T. herbarum grows on large dry stems of herbs.[10] The main method of transmission is by dissemination of the conidia components of this fungus making them present in the air.[11][6] Hyphal fragments of T. herbarum have been recovered from marine air above the Mediterranean Sea.[14] T. herbarum is frequently found on plant hosts in the genera: Alnus, Aceuthobium, Bambusa Carya, Impatiens, Juncus, Mesembryanthemum, Pinus, and Yucca.[11] Owing in part to their abundance in the air, conidia of T. herbarum contributing to seasonal fungal allergy in some people.[6] The weather and seasonal changes can affect how many conidia are present in the environment. The exposure of the fungal spores outdoors and indoors can lead to lower airway allergies.[15]

Physiology

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T. herbarum grows at temperatures of 24–28 °C (75–82 °F).[16] Growth is absent below -5 °C and above 37 °C.[16] T. herbarum is a secondary colonizer meaning it typically only establishes growth on a surface already subject to colonization by other fungi.[17] It is occurs in both aquatic and terrestrial ecosystems[18] subject to highly humid or even wet conditions.[17] T. herbarum is capable of decomposing soil and organic materials, including paper and can biodeteriorate marble.[6] It can breakdown lignin and decompose leaf litter.[18] T. herbarum was given the common name, "Herb Clinging Fibre" by Samuel Gray in 1821;[10] although few of Gray's many proposed common names for microfungi, including this one, were ever adopted.

A number of DNA sequences are available for this fungus including:[19][20][21][22]

Gene Partial Sequence Date of Identification Gene Accession Code
28S rRNA gene 853 bp linear DNA sequence Aug 19, 2018 LT963455
KNU17-5 large subunit ribosomal RNA gene 970 bp linear DNA sequence Apr 23, 2018 MH225777
CBS 246.57 large subunit ribosomal RNA gene 918 bp linear DNA sequence Nov 8, 2018 MH869251
HBUM07134 18S ribosomal RNA gene 1029 bp linear DNA sequence Jul 1, 2018 MF662283

T. herbarum forms the biocompounds, herabin and its derivatives, O-methylherbarin and dehydroherbarin.[7][23] Herbarin is a neutral compound with composition C16H16O6. Herbarin and dehydroherbarin possess weak antimicrobial effects and they are chemicals that belong to a class of pigments, where a Naphthoquinone moiety is fused with at positions 1 and 2 on an oxacyclohexene (chemical structure) ring.[23] O-methylherbarin is also a compound that belongs to the Naphthoquinone pigments.[24] Herbarone is a heptaketide that was also found to be produced by T. herbarum associated with a sea hare.[7]

Biotechnological application

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Torula herbarum produces several secondary metabolites like Herbarin, Dehydroherbarin, O-Methylherbarin.[25][24] Dehydroherbarin and herbarin displayed weak antibacterial, antifungal effects and antiamoebic activity for Entamoeba histolytica.[25] The compound dehydroherbarin was found to exhibit antimicrobial, antiparasitic, and phytotoxic effects.[4][16] Research has demonstrated dehydroherbarin to have antiviral activity for Hepatitis A virus.[4] It is antimicrobial to many species of bacteria including Staphylococcus aureus and Escherichia coli. Herbarin, did not show as strong of an antimicrobial ability.[4] When these two chemicals were tested for cytotoxicity, they showed a reduced effect towards the normal cell line but a higher effect against the breast cancer cells. Dehydroherbarin and herbarin bind to human heat shock protein 90 alpha and DNA Topoisomerase I through hydrogen bonds, 3 and 5 bonds, respectively, suggesting potential as anti-cancer agents.[4]

References

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  1. ^ a b c Scott, J. A.; Untereiner, W. A.; Ewaze, J. O.; Wong, B.; Doyle, D. (1 July 2007). "Baudoinia, a new genus to accommodate Torula compniacensis". Mycologia. 99 (4): 592–601. doi:10.3852/mycologia.99.4.592. PMID 18065010. S2CID 9099249.
  2. ^ Ellis, M.B.; Ellis, J.P. (1997). Microfungi on land plants : an identification handbook (2nd ed.). Richmond Pub. ISBN 9780855462468.
  3. ^ a b Hashmi, M. H.; Morgan-Jones, G.; Kendrick, Bryce (June 1973). "Conidium ontogeny in hyphomycetes. The blastoconidia of Cladosporium herbarum and Torula herbarum". Canadian Journal of Botany. 51 (6): 1089–1091. doi:10.1139/b73-137. ISSN 0008-4026.
  4. ^ a b c d e Osman, M.E.; El-Beih, A.A.; Khatab, O.-K.H.; Moghannem, S.A.M.; Abdullah, N.H. (July 2018). "Production of Herbarin and Dehydroherbarin by Endophytic Chaetosphaeronema sp. (KY321184) isolated from Nepeta septemcrenata and Evaluation of their Bioactivities". South African Journal of Botany. 117: 174–183. doi:10.1016/j.sajb.2018.05.018.
  5. ^ Kirk, Paul. "Torula Herbarum". Index Fungorum - Names Record. Index Fungorum Partnership.
  6. ^ a b c d e f g h i j k l m n Bogomolova, E. V.; Minter, D. W. (2003). "Torula herbarum. [Descriptions of Fungi and Bacteria]" (PDF). CABI Descriptions of Fungi and Bacteria (159).
  7. ^ a b c Geng, Wan-Li; Wang, Xian-You; Kurtán, Tibor; Mándi, Attila; Tang, Hua; Schulz, Barbara; Sun, Peng; Zhang, Wen (8 October 2012). "Herbarone, a Rearranged Heptaketide Derivative from the Sea Hare Associated Fungus". Journal of Natural Products. 75 (10): 1828–1832. doi:10.1021/np300642t. PMID 23043498.
  8. ^ a b c d e "Torula Herbarum". Fungi and Lichens of Great Britain and Ireland.
  9. ^ a b c d e f g h Crous, Pedro W.; Carris, Lori M.; Giraldo, Alejandra; Groenewald, Johannes Z.; Hawksworth, David L.; Hernández-Restrepo, Margarita; Jaklitsch, Walter M.; Lebrun, Marc-Henri; Schumacher, René K.; Stielow, J. Benjamin; van der Linde, Elna J.; Vilcāne, Jlija; Voglmayr, Hermann; Wood, Alan R. (1 June 2015). "The Genera of Fungi - fixing the application of the type species of generic names – G 2: Allantophomopsis, Latorua, Macrodiplodiopsis, Macrohilum, Milospium, Protostegia, Pyricularia, Robillarda, Rotula, Septoriella, Torula, and Wojnowicia". IMA Fungus. 6 (1): 163–198. doi:10.5598/imafungus.2015.06.01.11. PMC 4500082. PMID 26203422.
  10. ^ a b c Gray, Samuel Frederick (1821). A Natural Arrangement of British Plants: According to Their Relations to Each Other as Pointed Out by Jussieu, De Candolle, Brown, &c. ... London: Baldwin, Cradock, and Joy. p. 557.
  11. ^ a b c d Farr, David F.; Bills, Gerald F.; Chamuris, George P.; Rossman, Amy Y. (1989). Fungi on Plants and Plant Products in the United States (2nd ed.). St. Paul, Minn.: APS Press. p. 1252. ISBN 978-0890540992.
  12. ^ a b Tiwari, S. C.; Mishra, R. R. (July 1993). "Fungal abundance and diversity in earthworm casts and in uningested soil". Biology and Fertility of Soils. 16 (2): 131–134. doi:10.1007/BF00369414. ISSN 0178-2762. S2CID 21543667.
  13. ^ Nallathambi, P.; Umamaheswari, C. (2001). "A new disease of ber (Ziziphus mauritiana Lim) caused by Torula herbarum (Pers) link". Journal of Mycology and Plant Pathology. 31 (1). p. 92 ref. 3.
  14. ^ Gregory, P. H. (1973). The Microbiology of the Atmosphere (2nd ed.). USA & Canada: John Wiley & Sons. pp. 166–167. ISBN 978-0471-32671-7.
  15. ^ Knutsen, Alan P.; Bush, Robert K.; Demain, Jeffrey G.; Denning, David W.; Dixit, Anupma; Fairs, Abbie; Greenberger, Paul A.; Kariuki, Barbara; Kita, Hirohito; Kurup, Viswanath P.; Moss, Richard B.; Niven, Robert M.; Pashley, Catherine H.; Slavin, Raymond G.; Vijay, Hari M.; Wardlaw, Andrew J. (February 2012). "Fungi and allergic lower respiratory tract diseases". Journal of Allergy and Clinical Immunology. 129 (2): 280–291. doi:10.1016/j.jaci.2011.12.970. PMID 22284927.
  16. ^ a b c Kadkol, M. V.; Gopalkrishnan, K. S.; Narasimhachari, N. (1971). "Isolation and Characterization of Naphthaquinone Pigments from Torula Herbarum (Pers.). Herbarin and Dehydroherbarin". The Journal of Antibiotics. 24 (4): 245–248. doi:10.7164/antibiotics.24.245. PMID 5572751.
  17. ^ a b Hudson, H. J. (1992). Fungal biology. Cambridge: Cambridge University Press. p. 74. ISBN 978-0521427739.
  18. ^ a b Li, De-Wei (2016). Biology of Microfungi. Switzerland: Springer International Publishing. p. 299. ISBN 978-3-319-29135-2.
  19. ^ "Torula herbarum isolate KNU17-5 large subunit ribosomal RNA gene, part - Nucleotide - NCBI". www.ncbi.nlm.nih.gov. 2018-04-23.
  20. ^ "Torula herbarum strain CBS 246.57 large subunit ribosomal RNA gene, pa - Nucleotide - NCBI". www.ncbi.nlm.nih.gov. 2018-11-08.
  21. ^ "Torula herbarum genomic DNA sequence contains 28S rRNA gene - Nucleotide - NCBI". www.ncbi.nlm.nih.gov. 2018-08-19.
  22. ^ "Torula herbarum strain HBUM07134 18S ribosomal RNA gene, partial seque - Nucleotide - NCBI". www.ncbi.nlm.nih.gov. July 2018.
  23. ^ a b Nagarajan, R.; Narasimhachari, N.; Kadkol, M. V.; Gopalkrishnan, K. S. (1971). "Structure of Herbarin". The Journal of Antibiotics. 24 (4): 249–252. doi:10.7164/antibiotics.24.249. PMID 5572752.
  24. ^ a b NARASIMHACHARI, N.; GOPALKRISHNAN, K. S. (1974). "Naphthaquinone Pigments from Torula Herbarum: Structure of O-Methylherbarin". The Journal of Antibiotics. 27 (4): 283–287. doi:10.7164/antibiotics.27.283. PMID 4859426.
  25. ^ a b Cole, Richard J.; Schweikert, Milbra A. (2003). Handbook of Secondary Fungal Metabolites - Volume 1. USA: Academic Press. pp. 839–843. ISBN 978-0-12-179461-3.
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