Ascosphaera aggregata

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Ascosphaera aggregata
Ascosphaera journal.pone.0073419.g004.png
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Eurotiomycetes
Order: Onygenales
Family: Ascosphaeraceae
Genus: Ascosphaera
Species:
A. aggregata
Binomial name
Ascosphaera aggregata
Skou, JP (1975) [1]

Ascosphaera aggregata is a species of fungus.

History and taxonomy

Ascosphaera aggregata, discovered in 1975 by Jens-Peder Skou [1] is a fungus that is related to Ascosphaera apis . [2]

Contents

Habitat and ecology

Ascosphaera aggregata is an obligate parasite [3] that causes chalkbrood in bees, [4] symptom manifestations differ depending on age of the larva. [5] It primarily infects alfalfa leafcutting bees, Megachile rotundata . [2] [6] [7] [3] [8] Megachile rotundata infected with A. aggregata have been detected in the United States, Canada, [9] and South America. [5] Other bee species that A. aggregata has been seen to infect include the red mason bee ( Osmia rufa [8] ), the patchwork leafcutter bee ( Megachile centuncularis [8] ), Megachile pugnata and Megachile relativa . [2] [10] [8]

Growth, morphology and pathobiology

Ascosphaera aggregata is an obligate parasite that can cause chalkbrood by the fifth instar. [5] The majority of the life cycle and growth of A. aggregata occurs in M. rotundata larvae. Infection of bee larvae occurs only via ingestion of resting spores, [3] and is not possible via spore inhalation nor contact with the fungal vegetative form. [6] [5] Spores develop in the larva and cause it to swell, bursting the larval integument (giving the dead larvae a ragged appearance) [1] and furthering the spread of the fungus. Buildup of larval cadavers traps the unaffected emerging bees, forcing them to chew through the cadavers and be covered in spores. [7] Bees covered in spores then contaminate food provisions for other broods [7] and spread the infection.

Early vegetative growth utilizes gut lumen nutrients. [6] A. aggregata grows through the midgut wall to the hemocoele (event trigger is unknown, not because of lack of space nor food) [6] eventually replacing larval tissue. [3] Resulting larvae are filled with a mycelial mat comprising two layers: a dense inner layer and a less dense outer layer. [6]

Sexual development

Ascospore morphology consists of two layers: an inner chitinous and smooth layer, and an outer layer that is rough, spotted, [1] and not composed of chitin nor cellulose.; [6] ) Ascospore development in A. aggregata is unique and the resulting structure is referred to as a "spore cyst", or "ascocyst" or "synascus". [8] Sexual development occurs on the outer mycelial mat in the subcuticular region, [3] [6] and is documented to proceed as follows:

  1. The vegetative hyphae tips swell and form a thallus [6]
  2. The middle of the thallus grows and forms a nutriocyte (previously referred to as an archicarp [8] )
  3. The apical portion differentiates into the trichogyne cell. [6]
  4. Compatible trichogyne fuse and initiate plasmogamy. [6]
  5. Resulting dikaryotic fungal protoplasm then enters the nutriocyte and causes enlargement of the nutriocyte. [6]
  6. Nutriocyte growth causes the integument to rupture and initiate development of a fragile spherical structure without a cell wall. [6]
  7. Individual spores then pack together into a seemingly membrane-less spore ball. [11]
  8. Multiple spore balls then join and form a spore cyst. [11]
  9. Cell wall deposition changes spore colour from opaque white to grey to dull black [3] [6]

Physiology

Ascosphaera aggregata has been found to be unable to break down chitin. [6] [3]

Diagnostic considerations

Although ascospore development is very unique, it is very hard to identify A. aggregata because the spore balls and conidia tend to resemble other species. [12] Recent investigations by James and Skinner (2005) [12] have discovered that PCR of the ITS domain of ribosomal DNA with species specific primer sets allows the detection of fungal DNA (working, even, in asymptomatic individuals). [12] The PCR technique can also be used on hair and honey samples to avoid the difficulty of culturing spores, [12] as spore were shown before to only germinate well in lipids. [13] Storage of the fungus has also proven to be difficult as it collapses after 1–2 months during normal culture passaging. [14] However, Jensen et al. (2009) found that spores could be preserved via cryopreservation or freeze-drying whereas hyphae unfortunately could not be preserved. [14]

Economic importance

Megachile rotundata is the primary pollinator of the commercially grown alfalfa seed, [11] [7] accounting for 46,000 metric tonnes of North American alfafa seed (two-thirds the global production) in 2004. [7] M. rotundata is also the second most valuable field crop pollinator, behind the honey bee, because of the value of alfalfa in animal feed and hay. [7] A. aggregata has been killing this economic pollinator in the US since 1972 [10] and has been reported to be able to kill greater than 50% of a population. [8]

Effective management of the fungus has yet to be discovered, as the current registered treatment in Canada (paraformaldehyde fumigation of spores [7] ) involves a carcinogen and other treatment options (heat and chloride treatments) are expensive and labour-intensive. [7]

References

  1. 1 2 3 4 Skou, Jens-Peder (1975). "Two new species of ascosphaera and notes on the conidial state of Bettsia Alvei". Friesia. 11 (1): 62–74.
  2. 1 2 3 Goulson, Dave (2010). Bumblebees : behaviour, ecology, and conservation (2nd ed.). New York: Oxford University Press. p.  230. ISBN   978-0-19-955306-8.
  3. 1 2 3 4 5 6 7 Capinera, John L. (2008). Encyclopedia of entomology (2nd ed.). Springer. p.  304. ISBN   978-1-4020-6242-1.
  4. Tanada, Yoshinori; Kaya, Henry K. (1993). Insect pathology. California: Academic Press. p. 349. ISBN   0-12-683255-2.
  5. 1 2 3 4 Vandenberg, John D.; Stephen, W.P. (March 1982). "Etiology and symptomatology of chalkbrood in the alfalfa leafcutting bee, Megachile rotundata". Journal of Invertebrate Pathology. 39 (2): 133–137. Bibcode:1982JInvP..39..133V. doi:10.1016/0022-2011(82)90002-7.
  6. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 McManus, William R.; Youssef, Nabil N. (September 1984). "Life Cycle of the Chalk Brood Fungus, Ascosphaera aggregata, in the Alfalfa Leafcutting Bee, Megachile rotundata, and Its Associated Symptomatology". Mycologia. 76 (5): 830–842. doi:10.2307/3793139. JSTOR   3793139.
  7. 1 2 3 4 5 6 7 8 Pitts-Singer, Theresa L.; Cane, James H. (7 January 2011). "The Alfalfa Leafcutting Bee, Megachile rotundata: The World's Most Intensively Managed Solitary Bee". Annual Review of Entomology. 56 (1): 221–237. doi:10.1146/annurev-ento-120709-144836. PMID   20809804. Archived from the original on 11 June 2020.
  8. 1 2 3 4 5 6 7 Bissett, John (December 1988). "Contribution toward a monograph of the genus". Canadian Journal of Botany. 66 (12): 2541–2560. doi:10.1139/b88-346.
  9. Rank, GH; Goerzen, DW (1981). "Native leafcutter bee species and associated parasites in commercial hives in Saskatchewan, Canada". Apidologie. 12 (3): 211–220. doi: 10.1051/apido:19810301 .
  10. 1 2 Goerzen, D.W.; Erlandson, M.A.; Bissett, J. (31 May 2012). "Occurrence of Chalkbrood Caused by Ascosphaera Aggregata Skou in a Native Leafcutting Bee, Megachile Relativa Cresson (Hymenoptera: Megachilidae), in Saskatchewan". The Canadian Entomologist. 122 (6): 1269–1270. doi:10.4039/Ent1221269-11. S2CID   85760024.
  11. 1 2 3 Richards, K.W. (31 May 2012). "Detection of a Chalkbrood Fungus, Ascosphaera Aggregata, in Larvae of the Alfalfa Leafcutter Bee (Hymenoptera: Megachilidae) from Western Canada". The Canadian Entomologist. 117 (9): 1143–1145. doi:10.4039/Ent1171143-9. S2CID   84474941.
  12. 1 2 3 4 James, R. R.; Skinner, J. S. (1 October 2005). "PCR diagnostic methods for Ascosphaera infections in bees". Journal of Invertebrate Pathology. 90 (2): 98–103. Bibcode:2005JInvP..90...98J. doi:10.1016/j.jip.2005.08.004. ISSN   0022-2011. PMID   16214164.
  13. James, R. R.; Buckner, J. S. (1 October 2004). "Lipids stimulate spore germination in the entomopathogenic ascomycete Ascosphaera aggregata". Mycopathologia. 158 (3): 293–302. doi:10.1007/s11046-004-2910-5. ISSN   1573-0832. PMID   15645171. S2CID   21838968.
  14. 1 2 Jensen, A. B.; James, R. R.; Eilenberg, J. (1 June 2009). "Long-term storage of Ascosphaera aggregata and Ascosphaera apis, pathogens of the leafcutting bee (Megachile rotundata) and the honey bee (Apis mellifera)". Journal of Invertebrate Pathology. 101 (2): 157–160. Bibcode:2009JInvP.101..157J. doi:10.1016/j.jip.2009.03.004. ISSN   0022-2011. PMID   19332075.