Lactarius Indigo

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1. Classification

a. Higher order taxa

The organism Lactarius indigo belongs to the domain Eukarya, the phylum Basidiomycota, the class Agaricomycetes, the order Russulales, the family Russulaceae, and the genus Lactarius [1].

2. Description and significance

Species

Originally, this species was recognized as Agaricus Indigo by American mycologist Lewis David de Scheinitz, but was later transferred to the genus Lactarius in 1838 [2]. There was some controversy surrounding the identification and naming of the mushroom as early mycologists believed that the mushroom's blue milk and stick blue cap classified the mushroom under the subgenus Caerulei [3]. In the late 1970s, they revised their opinions on the basis of the characteristics of the milk, which changed color from blue to green, and subsequently moved the mushroom to the subgenus Lactarius [3]. Today, this particular mushroom is recognized as a species of agaric fungus that is specifically known under the Lactarius genus, as the species of Lactarius indigo.

Introduction

Lactarius indigo, also known as the blue milk mushroom, is a fungus that is found throughout areas of eastern North America, East Asia, and Central America [3]. Like many other mushrooms, L. indigo fruit bodies develop from a nodule that forms within the underground mycelium, a group of threadlike fungal cells referred to as hyphae, that make up the majority of the organism [3]. The mushroom is known widely for its edibility and is sold at many markets found in the areas where these fungi grow. The flesh of the mushroom is a pale blue color and its taste can be mild to slightly acidic, while also having a grainy texture. The milk of the mushroom is indigo blue, but turns green upon exposure to the air and is reported to have a mild taste as well [3]. Current research has indicated the mycorrhizal ability of L. indigo can prove useful in reforestation efforts [4], although it is unclear if the fungus can make significant impacts in the context of an entire forest. L. indigo is a popular delicacy in the native areas it grows, leading it to be a secure source of income for the locals that sell these mushrooms [5]. The dietary benefits of this mushroom include being a large source of dietary fiber and low in fat content compared to other mushrooms in similar specimens [6]. There has been some preliminary evidence that also suggests L. indigo has antibacterial properties and has the potential to be used in pharmacological studies [7].

3. Genome structure

Lactarius indigo’s genome is being sequenced by the Joint Genome Institute as of early 2020. The transcriptome of the fungus was sequenced with Illumina technology in year 2020 [8]. The average gene length is about 1695 base pairs, with 232 exons, 70 introns, and 1,361 gene transcripts [8]. The genome contains 11,643 multigene clusters, each cluster having an average size of 13.44 [8].

4. Cell structure

Lactarius indigo is multicellular, eukaryotic and forms a network of threadlike fungal cells called hyphae [3]. The fungus is a heterotrophic organism that feeds off decaying matter on the forest floor [3]. The mushroom of L. indigo is characterized by its small blue stem, large blue zonated cap, and acrid tasting blue latex production [9]. The spores that are found in the fungus appear as a creamy yellow color and are spherical in shape [3]. The most prominent features of this particular fungus include its striking blue cap and blue milk that accompanies it; the cap of the mushroom can measure from 5-15 cm in diameter and is initially convex before it ages and becomes more depressed and funnel shaped [3].

5. Metabolic processes

Fungi have a range of complex metabolic processes allowing them to decompose organic matter, classifying Lactarius indigo as a chemoheterotroph [10]. L. indigo is made up of many essential compounds that attribute to its edible properties. It contains 4.3 mg/g of fat, 13.4 mg/g of protein, and 18.7 mg/g of dietary fiber. Compared to the other wild mushrooms tested, L. indigo was also found to have the highest levels of saturated fatty acids, such as stearic acid [6]. The Indigo Milk Cap’s distinct bright blue color is due to an organic analogous compound to azulene [11].

6. Ecology

Lactarius indigo is found in the soil of oak and pine forests [12] and forms ectomycorrhizal relationships with pine trees in North America, Europe, and Asia [4]. L. indigo has been observed in Northeast and Central America, and is particularly abundant in Mexico and Guatemala [4]. L. indigo grows during the wet season between June and September in the Northern hemisphere [13].

7. Pathogenicity

Lactarius indigo does not cause disease and is non-poisonous [13]. Lactarius indigo is known for its edibility and is ranked in Mexico as one of the top three mushrooms using the Edible Mushrooms Cultural Significant Index [13]. L. indigo is sold in markets and is consumed frequently in the rainy season [12]. The criteria people use to determine mushroom edibility is by ensuring the mushroom doesn’t turn purple or green when cut, there is a pleasant odor and taste, and the cap doesn’t have scales [12]. Lactarius indigo can be confused with Omphalotus mexicanus, which is similar in appearance, but is pathogenic and will cause vomiting and diarrhea [13].

8. Ethnomycology

Lactarius indigo is culturally significant and contributes to the history and sociology of certain groups. People of Tlaxcala refer to Lactarius indigo in their native language of Náhuatl as “cacaxnanácatl”, referring to its blue appearance. L. indigo plays a role in commerce and consumption through being sold in Mexican farmers markets [12]. The blue milk mushroom has a high Frequency of Use Index (FUI) and a high Knowledge Transmission Index (KTI), demonstrating its functionality and likelihood of being shared by one’s ancestors [13]. Transferring fungal knowledge and collecting mushrooms strengthens families ties, causing L. indigo and other mushrooms to be an integral part of indigenous culture [13].

9. Current Research

Ectomycorrhizal Associations

With Lactarius indigo’s ability to form ectomycorrhizal interactions with pine and oak species, research has been conducted to analyze the effect of these interactions on host tree growth. One study found mycorrhizal associations to be successful even in neotropical pine species whose associations have not yet been found to occur in natural Guatemalan ecosystems [4]. Although further research needs to be conducted, this ability of L. indigo to form mycorrhizal associations that do not occur naturally in ecosystems may be important for future reforestation efforts, particularly in Central America [4]. Another study found L. indigo to have a higher mushroom density in both pine and oak forests compared to that of Cupressus lusitanica plantations, which only contained one dominant tree species that did not form ectomycorrhizal associations [14]. Since these plantations are a common method used for restoring forests and for collecting timber, adding ectomycorrhizal host trees like pines and oaks may help improve these plantations’ ecosystems, by allowing for a larger diversity and abundance of wild edible mushrooms, such as L. indigo, to grow [14].

Antibacterial Properties

The major role of L. indigo in the world is in culinary practices. It is known for its mesmerizing color and the cultural significance it has in countries such as Mexico [12]. However, research has indicated the mushroom has antibacterial and cytotoxic properties [7]. Bioassays and cytotoxic assays were created to compare the inhibition of strains with only hexane and methanol versus with the Lactarius indigo. When tested against different bacteria, such as diarrheagenic Escherichia coli strains, the L. indigo inhibited proliferation of certain pathogenic bacteria [7]. The inhibitory effect depended on the bacteria it was tested against and the dosage of L. indigo [7]. Overall, the study indicated possible medicinal properties in L. indigo [7].

10. References

[1] Taxonomy browser 2020. https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Undef

[2] De Schweinitz LD. 1832. “Synopsis fungorum Carolinae superioris.” Schriften der naturforschenden Gesellschaft in Leipzig (in Latin). 1:87.

[3] Kuo, M. 2011. Lactarius Indigo. https://mushroomexpert.org.

[4] Flores, R., G. Díaz, and M. Honrubia. 2005. Mycorrhizal synthesis of Lactarius indigo (Schw.) Fr. with five Neotropical pine species. Mycorrhiza 15: 563–570.

[5] Guy, T. 2020. Lactarius Indigo: The Indigo Milk Cap Identification. https://healing-mushrooms.net/indigo-milk-cap

[6] León-Guzmán, M. F., I. Silva, and M. G. López. 1997. Proximate Chemical Composition, Free Amino Acid Contents, and Free Fatty Acid Contents of Some Wild Edible Mushrooms from Queretaro, Mexico. Journal of Agriculture and Food Chemistry 45 (11): 4329-4332.

[7] Zarzosa, A. O., S. V. Garcidueñas, V. A. R. Fuentes, and G. V. Marrufo. 2011. Antibacterial and cytotoxic activity from basidiocarp extracts of the edible mushroom Lactarius indigo (Schw.) Fr. (Russulaceae). African Journal of Pharmacy and Pharmacology 5(2): 281-288.

[8] JGI: The Fungal Genomics Resource 2020. https://mycocosm.jgi.doe.gov/Lacind1/Lacind1.info.html

[9] Hesler, L. R., and A. H. Smith. 1960. Studies on Lactarius-I: The North American Species of Sect. Lactarius. Britonia 12.2: 119-39.

[10] Greene, G. H., K. L. McGary, A. Rokas, and J. C. Slot. 2014. Ecology drives the distribution of specialized tyrosine metabolism modules in fungi. Genome Biology Evolution 6: 121–132.

[11] Harmon, A.D., K.H. Weisgraber, and U. Weiss. 1980. Preformed azulene pigments of Lactarius indigo (Schw.) Fries (Russulaceae, Basidiomycetes). Experientia 36 (1): 54-56.

[12] Montoya, A., O. Hernández-Totomoch, A. Estrada-Torres, A. Kong, and J. Caballero. 2003. Traditional knowledge about mushrooms in a Nahua community in the state of Tlaxcala, México. Mycologia 95 (5): 793–806.

[13] Robles-Garcia, D., H. Suzan-Azpiri, A. Montoya-Esquivel, J. Garcia-Jimenez, E. U. Equivel-Naranjo, E. Yahia, and F. Landeros-Jaime. 2018. Ethnomycological knowledge in three communities in Amealco, Queretaro, Mexico. Journal of ethnobiology and ethnomedicine 14:7.

[14] Torres-Gómez, M., R. Garibay-Orijel, A. Casas, and D. R. Pérez-Salicrup. 2018. Ectomycorrhizal trees intermingled within Cupressus lusitanica plantations sustain the diversity and availability of edible mushrooms. Agroforestry Systems 92 (2): 575-588.

Edited by Tiffany Leigh, student of [mailto:jmbhat@bu.edu Jennifer Bhatnagar] for [http://www.bu.edu/academics/cas/courses/cas-bi-311/ BI 311 General Microbiology], 2020, Boston University.