Journal of Industrial Microbiology. Y (1992) 149-161
IYY2 Society for Industrial Microbiology 0169-4146'92'505.00
Published by Elsevier
Insect fungal symbionts: a promising source of detoxifying
Patrick F. Dowd
Mycotoxin Research Unit. National Centerfor Agricultural Utilization Research. U.S.D.A.• Agriculrural Research Service. Peoria. Illinois.
(Received 24 June 1991; revision received 9 December 1991; accepted 12 December 1991)
Key words: Toxin; Secondary plant metabolite; Allelochemical; Insecticide; Mycotoxin; Endocylobiont
Many species ofinsects cultivate. inoculate. or contain· symbiotic fungi. Insects feed on plant materials that contain plant-produced defensive tOXins.
or are exposed to insecticides or other pesticides when they become economically imponant pests. Therefore, it is likely that the symbiotic fungi are also
exposed to these toxins and may actually contribute to detoxification ofthese compounds. Fungi associated with bark beetles. ambrosia beetles. termites.
leaf-cutting ants. long-horned beetles. wood wasps. and drug store beetles can variously metabolize/detoxify tannins.lignins. terpenes, esters, chlorinated
hydrocarbons. and other toxins. The fungi (Allamyces) cultivated by the ants and the yeast (Symbiolaphrina) contained in the cigarette beetle gut appear
to have broad-spectrum detoxifying abilities. The present limiting factor for using many of these fungi for large scale detoxification of. for example.
contaminated soils or agricultural commodities is their slow growth rate. but conventional strain selection techniques or biotechnological approaches should
overcome this problem.
At a time when environmental concerns have been
highlighted, the search for detoxifyingenzymes has greatly
expanded. Microorganisms have shown promise in decon-
taminating some pesticide residues and agricultural com·
modities such as oil seed meals. However, in many cases
these microorganisms can onlydetoxify a single. or closely
related toxins. In addition, there are many toxins for
which no effective detoxifying microorganism or other
process is available. Thus, there is still a need for micro-
organisms or other sources of new detoxifying enzymes.
preferably with good stability and broad·spectrum detoxi-
fying ability. In this review, fungal insect symbionls will be
considered as a source of detoxifying enzymes. The dis-
cussion will begin with a review ofthe types, distribution
and species of insects and fungi involved in symbiotic
Correspondence: P.F. Dowd, USDA·ARS, 1815 N. University
St., Peoria, IL 61604, U.S.A.
* Presented at the Symposium on Fungal Detoxification at the
48th Annual Meeting ofthe Society for Industrial Microbiology,
Philadelphia, PA, August 4-9, 1991.
relationships. The discussion will continue by considering
why insect symbionts might produce detoxifying enzymes.
reactions from the different types of symbioses will be
described. Finally, the feasibility ofusing these symbionts
for detoxification will be explored.
INSECT FUNGAL SYMBIONTS
In the less highly evolved relationships, It IS often
difficult to determine ifa microorganism associated with
an insect is a symbiont. The presence of saprophytes in
confounded matters (see below). In addition, the fungi
that act as symbiotic partners of insects are varied in
regard to the intimacy ofthe association. The number of
diagnostic tests that cal! be performed on the fungi, due
to their oftentimes obligate relationship, is frequently
limited. These limitations often result in a particular
fungus being classified in a variety ofways. Two extremes
appear to be morphological co·identity, where the fungi
are identified as free·living species, and symbiosis iden·
tity, where all symbionts from the same insect species are
classified as unique species, and those from related insects
o Indicates fungi are associated with insects, but status as
symbionts is unknown or uncertain.
Hosts and genera of fungal insect symbionts
[7. 3 ~ . 50J
[7. 3 ~ . 50J
[7. 3 ~ . 50J
[7. 3 ~ J
[ 3 ~ J
( 3 ~ . 50j
[ 3 ~ J
[ 3 ~ . 50J
[ 3 ~ ]
Bark beetles (Ips)
Ants (Formicidae: Auinae)
Drug store beetles
Sap beetles (Nitidulidae)
Cicadas and relatives
(Cerambycidae - some genera)
Homtails and wood wasps
(Siricidae and Xyphrydiidae)
Scale Insects (Coccoidea)
Extracorporeal Associations - Inoculators
Fruit files (Drosophilidae)
Extracorporeal Associations - Cultivators
are put in the same genus. The intent ofthis paper is not
to offer yet another view on this problem. Recent success
in molecular taxonomy of fungi hopefUlly will soon be
applied to insect fungal symbionts and thereby clarify
taxonomic relationships. The majority of the following
material has been compiled from reviews. The reader is
advised to check recent taxonomic fungal compendia for
One type of symbiotic association is where the rela-
tionship is extracorporeal and insects serve as inoculators
(Table 1). For these insects, it is sometimes difficult to
determine which fungi are symbionts, and which are
casual associates. Bark beetles (Coleoptera: Scolytidae)
bore into and feed on the vascular phloem (bark) tissue
ofwoody plants , and sometimes may kill trees [7, 145].
Ambrosia beetles (Coleoptera: Scolytidae and Platy-
podidae) are so-called because of the growth patterns of
the fungi they inoculate and subsequently feed upon in the
xylem of dead tress or other woody plants [7, 50]. The
larvae of horntails (Hymenoptera: Siricidae) and wood
wasps (Hymenoptera: Xyphriydiidae) feed on dead or
.Ship timber worms (Coleoptera:
Lyxmelidae) also feed on wood . Other insects that
may inoculate fungi include detritivorous sap beetles
(Coleoptera: Nitidulidae) [39, 98], cactus-feeding fruit
flies (Diptera: Drosophilidae) , adult lacewings
(Neuroptera: Chrysopidae) , and some dung beetles
(Coleoptera: Scarabaeidae) . Some scale insects are
shielded with fungi that invade the body cavity, but not
individual cells . Other associations that may evolve
into symbiotic relationships include cases where insects
are known consumers of mushrooms , Ascomycetes
, or yeast .
Some insects appear to actively cultivate, and then
consume, their symbiotic fungi. Some termites that
inhabit Africa and Asia build nests in soil that extend
mound-shaped from the earth [6, 149]. The fungi form
spherules as they grow on masticated woody material
and/or primary feces ofthe termites . Fungus-growing
ants aredistributed in South,Central, and North America
and also build nests in the ground that may also form
mounds. The fungi form swellings (gongylidiae) as they
grow on masticated plant debris, insect frass. or fresh
plant material . Adults primarily feed on plant sap
, and use the fungal growths to feed the larvae .
Although intracellular bacterial symbionts appear
more common, many species ofinsects also contain intra-
cellular symbiotic fungi. Several families of scale insects
(Coccoidea), plant hoppers (Fulgoroidea), and cicada-
like insects (Cicadoidea) all of which are sap feeders,
contain symbiotic yeasts which have not been identified.
Intracellular yeasts are also found in certain genera 
of the longhorned beetles (Coleoptera: Cerambycidae),
1)7 Meyer. S.A.. D.G. Ahearn and D. Yarrow. 1984. Genus 4.
Candida Berkhout.ln: The Yeasts (Kreger-van Rij, N.I.W..
ed.) 585-844. Academic Press, New York, NY.
98 Miller. M.W. and E.M. Mrak. 1954. Yeasts associated with
dried-fruit beetles in figs. AppL Environ. MicrobioL I:
99 Mishra. S.c. and P.K. Sen-Sarma. 1985. Carbohydrases in
Scarabaeidae) and their evolutionary significance. Mater.
Organ. 20: 221-230.
100 Mishra. S.c. and P. Singh. 1978. Polysaccharide digestive
enzymes in the larvae ofStromatium barbatum (Fabr.), a dry
wood borer(Coleoptera: Cerambycidae). Mater. Organ. 13:
101 Mitscher, L.A., W.W. Andres, G.O. Morton and E.L.
endo-ethenotetrahydrothebaine alkaloids. Experientia 24:
102 Morgan, E.D. and M.D. Thorton. 1973. Azadirachtin in the
fruit of Melia Azedarach. Phytochemistry 12: 391-392.
103 Morrow, P.A. and L.R. Fox. 1980. Effects of variation in
Euca(l'ptus essential oil yield on insect growth and grazing
damage. Oecologia (Berl.) 45: 209-219.
104 Muller, W. 1934. Untersuchungen iiber die Symbiose von
Tieren mit Pilzen und Bakterien. Arch. MikrobioL 5:
105 Nardon. P. and A.M. Grenier. 1989. Endosymbiosis in
Coleoptera: Biological, biochemical and genetic aspects. In:
Insect Endocytobiosis. (Schwemmler, W. and G. Gassner.
eds.) 175-215. CRC Press, Boca Raton, FL.
106 Osore, H. 1985. The role of microorganisms isolated from
fungus-comb-constructing African termites in the degrada-
tion of lignocellulose. In: Energy from Biomass (Palz, W.,
Coombs, J. and Hall, D.O., eds.) 999-1000. Elsevier, New
107 Osore, H. 1987. Lignocellulose decomposition by fungi iso-
lated from the fungus garden of Macrotermitinae group of
higher African termites. In: Biomass Conversion Tech-
nology (Moo-Young, M., J. Lamptey, B. Glick and H.
Bungay, eds.) 19-26. Pergamon Press, New York, NY.
108 Osore, H. and M.A. Okech. 1983. The partial purification
and some properties of cellulase and P-glucosidase of
Termilomyces conidiophores and fruit bodies. J. Appl.
Biochem. 5: 172-179.
109 Palo, R.T. 1984. Distribution of birch (Betula spp.). willow
(Salix spp.) and poplar (Populus spp.) secondary metabo-
lites and their potential role as chemical defense against
herbivores. J. Chern. EcoL 10: 499-520.
110 Powell, R.I. 1984. The influence of substrate quality on
fungus cultivation by some attine ants. Ph. D. Thesis.
University of Exeter, UK.
III Quinlan, RJ. and J.M. Cherrett. 1978. Aspects of the
symbiosis of the leaf-cutting ant Acromyrmex oClOspinosus
(Reich) and its food fungus. EcoL EntomoL 3: 221-230.
112 Raffa, K.F. and A.A. Berryman. 1987. Interacting selective
pressures in conifer-bark beetle systems: a basis for recipro-
cal adaptations? Am. Nat. 129: 234-262.
113 Raffa. K.F., A.A. Berryman, J. Simasko, W. Teal and B.L.
\Vong. 11)85. Effects of grand fir monoterpenes on the fir
engraver. SCO(VIUS ventralis (Coleoptera: Scolytidae). and its
symbiotic fungus. Environ. EntomoL 14: 552-556.
114 Rao, K.D.P., D.M. Norris and H.M. Chu. 1979. Lipid inter-
dependencies between Xyloborus ambrosia beetles and their
ectosymbiotic microbes. In: Metabolic Aspects of Lipid
Nutrition in Insects (Mittler, T.E. and R.H. Dadd, eds.)
27-40. Westview Press, Boulder, CO.
115 Reid, R.W. 1970. Effect oftemperature and resin on hatch
of eggs of the mountain pine beetle (DendroclOnus pon-
derosae). Can. EntomoL 102: 617-622.
116 Robbins, C.T., T.A. Hanley, A.E. Hagerman, O. Hjeljord,
D.L. Baker, C.c. Schwartz and W.W. Mautz. 1987. Role of
tannins in defending plants against ruminants: reduction in
protein availability. Ecology 68: 98-107.
117 Rohrmann, G.F. and A.Y. Rossman. 1980. Nutrient strate-
gies of Macrotermes ukuzii (Isoptera: Termitidae). Pedo-
biologia 20: 61-73.
118 Rosenthal, G.A. and D.H. Janzen. 1979. Herbivores: Their
Interaction with Secondary Plant Metabolites. Academic
Press, New York, NY.
119 Sands.W.A. 1969.The association oftermites and fungi. In:
Biology ofTermites (Krishna, K. and F.M. Weesner, eds.)
495-524. Academic Press, New York, NY.
120 Schlottke, E. 1945. Dber die Verdauungsfermente in Holz
fressender Kiiferlarven. ZooL PhysioL Tiere. 61: 88-140.
121 Schwartz, W. 1924. Untersuchungen iiber die Pilzsymbiose
der Schildlause. BioI. ZentralbL 44: 487-495.
122 Scriber, J.M. and F. Siansky, Jr. 1981. The nutritional
ecology of immature insects. Ann. Rev. EntomoL 26:
123 Seaman, F.C. 1984. The effects of tannic acid and other
phenolics on the growth of the fungus cultivated by the
leaf-cutting ant, Myrmicocrypta buenzlii. Biochem. Syst.
EcoL 12: 156-158.
124 Shen, S.K. and P.F. Dowd. 1989. Xenobiotic induction of
esterases in cultures of the yeast-like symbiont from the
cigarette beetle. EntomoL Exp. AppL 52: 179-184.
125 Shen, S.K. and P.F. Dowd. 1991. I-Naphthyl acetate ester-
ase activity from cultures of the symbiont yeast of the
cigarette beetle (Coleoptera: Anobiidae). J. Econ. EntomoL
126 Shen. S.K. and P.F. Dowd. 1991. Detoxification spectrum
of the cigarette beetle symbiont Symbiolaphrina kochii in
culture. EntomoL Exp. AppL 60: 51-59.
127 Shigo, A.L. and W.E. Hillis. 1973. Heartwood, discolored
wood. and microorganisms in living trees. Annu. Rev.
Phytopath. 11: 197-222.
128 Singh. B.• P.K. Agrawal and R.S. Thakur. 1989. An acyclic
triterpene from Phyllanthus niruri. Phytochemistry 28:
129 Stamopoulos, D.C. 1988. Toxic effects of lignin extracted
from the tegument ofPhaseolus vulgaris seeds on the larvae
ofAcanrhoscelides obleclus (Say) (Col. Bruchidae). J. AppL
EntomoL 105: 317-320.
130 Starmer, W.T. and J.c. Fogleman. 1986. Coadaptation of
Drosophila and yeasts in their natural habitat. J. Chern. EcoL
131 Swain. T. 1979. Tannins and lignins. In: Herbivores: Their
Interactions with Secondary Plant Metabolites (Rosenthal,
G.A. and D.J. Janzen, eds.) 657-682. Academic Press, New
132 Tempesta, M.S., D.G. Corley, J.A. Beutler, C.J. Metral,
R.A. Yunes, CA. Giacomozzi and J.B. Calixto. 1988.
Phyllanthimide, a new alkaloid from Phyllanthussellowianus.
J. Nat. Prod. 51: 617-618.
133 Therrien, P., J.N. McNeil, W.G. Wellington and G. Febvay.
1986. Ecological studies ofthe leaf-cutting ant, Acromyrmex
oClOspinosus, in Guadeloupe. In: Fire Ants and Leaf-Cutting
Ants:Biology andManagement (Loffren, CS., ed.)
172-183. Westview Press, Boulder, CO.
134 Thomas, RJ. 1981. Ecological studies on the symbiosis of
TermilOmyces Heim with Nigerian Macrotermitinae. Ph. D.
Thesis, Univ. London, U.K.
135 Trembley. E. 1989. Coccoidea endocytobiosis. In: Insect
Endocytobiosis (Schwemmler, W. and G. Gassner, eds.)
145-173. CRC Press, Boca Raton, FL.
136 van Emden. H.F. 1982. Aphids as phytochemists. In:
Biochemical Ecology (Harborne. J.. ed.) 25-43. Academic
Press. New York. NY.
137 van Etten. CH. and H.L. Tookey. 1979. Chemistry and
biological effects of glucosinolates. In: Herbivores: Their
Interaction with Secondary Plant Metabolites (Rosenthal.
G.A. and D.H. Janzen. eds.) 471-501. Academic Press.
New York, NY.
138 Van Etten. H.. D.E. Matthews and P.S. Matthews. 1989.
Ph}10alexin detoxification: importance for pathogenicity
and practical implications. Annu. Rev. Phytopatho!. 27:
139 Wainhouse. D., DJ. Cross and R.S. Howel!. 1990. The role
of lignin as a defence against the spruce bark beetle
Dendrocronus micans: effect on larvae and adults. Oecologia
140 Waller, D.A. 1986. The foraging ecology of Allu rexullu in
Texas. In: Fire Ants and Leaf-Cutting Ants: Biology and
Management. (Lofgren, CS., ed.) 146-158. Westview
Press, Boulder. CO.
141 Wallnofer. P.R.. O. Hutzinger. G. Engelhardt and \\'.
Ziegler. 1984. Microbial transformations of pesticides. In:
Handbook of Microbiology. Volume VII. (Laskin. A.1. and
H.A. Lechevalier. eds.) 491-558. CRC Press. Boca Raton.
142 Weber, N.A. 1979. Fungus-culturing by ants. In: Insect-
Fungus Symbiosis (Batra, L.R., ed.) 77-115. Allanheid.
Osmun Press, Montclair, NJ.
143 Weston, RJ. 1984. Eucalyprus oils in larvae ofgum emperor
moth, Antheraea euca(vpri. J. Chern. Eco!. 10: 1489-1496.
144 Whitney, H.S. 1982. Relationships between bark beetles
and symbiotic organisms. In: Bark Beetles in North Ameri-
can Conifers (Mitton, J.B. and K.B. Sturgeon, eds.)
183-211. University of Texas Press, Austin, TX.
145 Whitney, H.S. and F.W. Cobb, Jr. 1972. Non-staining fungi
associated with the bark beetle DendroclOnus brevicomis
(Coleoptera: Scolytidae)on Pinusponderose. Can. J. Bot. 50:
146 Wilson, E.O. 1986. The defining traits of fire ants and leaf-
cutting ants. In: Fire Ants and Leaf-Cutting Ants: Biology
and Management. (Lofgren, CS. ed.) 1-9. \Vestview Press,
147 Wink, Moo T. Hartmann, L. Witte and J. Rheinheimer. 1982.
Interrelationship between quinolizidine alkaloid producing
legumes and infesting insects: exploitation of the alkaloid-
containing phloem sap of Cyrisus scoparius by the broom
aphid Aphis cyrisorum. Z. Naturforsch. 370: 1081-1086.
148 Wong, S.M., M.M. Wong, O. Seligmann and H. Wagner.
1989. Anthraquinone glycosides from seeds of Cassia lOra.
Phytochemistry 28: 211-214.
149 Wood. T.G. and RJ. Thomas. 1989. The mutualistic asso-
ciation between Macrotermitinae and Termilomyces. In:
Insect-Fungus Interactions (Wilding, N., N.M. Collins,
P.M. Hammond and J.F. Webber, eds.) 69-92. Academic
Press. New York, NY.
150 Yamada. H. and S. Shimizu. 1988. Microbial and enzymatic
processes for the production ofbiologically and chemically
useful compounds. Angew. Chern. Int. Ed. Eng!. 27: