Riding with the ants

Isolates of Teratosphaeriaceae have frequently been found in the integument of attine ants, proving to be common and diverse in this microenvironment. The LSU phylogeny of the ant-isolated strains studied revealed that they cluster in two main lineages. The first was associated with the genus Xenopenidiella whereas the other represented two ant-isolated lineages sister to the taxa Penidiella aggregata and P. drakensbergensis, which are allocated to the new genus Penidiellomyces. The genus Penidiella is limited to the lineage containing P. columbiana, which is not congeneric with Penidiellomyces or Penidiellopsis, nor with Simplicidiella, a novel genus introduced here to accommodate a strain isolated from ants. For species level analysis, the final 26 aligned sequences of the ITS (498 characters), cmdA (389 characters), tef1 (342 characters) and tub2 (446 characters) gene regions lead to the introduction of six new species in Xenopenidiella, and one in respectively Penidiellopsis and Simplicidiella. The species described in this study were distinguished by the combination of morphological and phylogenetic data. Novelties on the integument of leaf-cutting ants from Brazil include: Penidiellopsis ramosus, Xenopenidiella clavata, X. formica, X. inflata, X. laevigata, X. nigrescens, X. tarda spp. nov., and Simplicidiella nigra gen. & sp. nov. Beta-tubulin is recommended as primary barcode for the distinction of species in Penidiellopsis, whereas ITS was sufficient to distinguish species of Xenopenidiella.FAPESP (São Paulo Research Foundation; grant 2013/08540-4) and CNPq (National Council for Scientific and Technological Development; grants number: 560.682/2010-7 and 448941/2014-7).http://www.persoonia.orghttp://www.ingentaconnect.com/content/nhn/pimjam2017Forestry and Agricultural Biotechnology Institute (FABI)Microbiology and Plant Patholog

Cryptococcus haglerorum, sp. nov., an anamorphic basidiomycetous yeast isolated from nests of the leaf-cutting ant Atta sexdens.

A yeast strain (CBS 8902) was isolated from the nest of a leaf-cutting ant and was shown to be related to Cryptococcus humicola. Sequencing of the D1/D2 region of the 26S ribosomal DNA and physiological characterization revealed a separate taxonomic position. A novel species named Cryptococcus haglerorum is proposed to accommodate strain CBS 8902 that assimilates n-hexadecane and several benzene compounds. Physiological characteristics distinguishing the novel species from some other members of the C. humicola complex are presented. The phylogenetic relationship of these strains to species of the genus Trichosporon Behrend is discussed

Growth of symbiont fungi of some higher attine ants in mineral medium Crescimento do fungo simbionte de alguns attine superiores em meio mineral

Bioassays were conducted to verify the possibility of culturing the symbiont fungus of some higher attine in mineral medium and finding out the optimum pH value for their satisfactory mycelial growth. Three organic media and one mineral medium were inoculated with isolates from Atta sexdens piriventris and Acromyrmex heyeri. In mineral medium different values of pH (4.0, 5.0, 6.0 and 7.0) were tested with isolates from A. laevigata and A. laticeps. The behavior of isolates (colony diameter) was different in the mineral medium. However, even the one which grew the least of all provided enough mycelial for RAPD analysis. The best range of pH for fungal growth in mineral medium was between 4.0 and 5.0<br>Foram conduzidos bioensaios para verificar a possibilidade de cultivar o fungo simbionte de alguns attine superiores em meio mineral e obter um valor de pH ótimo para o seu crescimento micelial. Três meios orgânicos e um meio mineral foram testados, avaliando-se o crescimento (diâmetro da colônia) de isolados de fungos de Atta sexdens piriventris e Acromyrmex heyeri. No meio mineral, diferentes valores de pH (4,0, 5,0, 6,0 and 7,0) foram avaliados, por meio do mesmo parâmetro anterior, com isolados de fungos de A. laevigata e A. laticeps. No meio mineral, os isolados testados apresentaram crescimento diferenciado, entretanto mesmo aquele que menos cresceu, forneceu material suficiente para as análises de RAPD. No mesmo meio, verificou-se que a melhor faixa de pH para o crescimento micelial está entre 4,0 e 5,0

Occurrence of Killer Yeasts in Leaf-Cutting Ant Nests

Killer activity was screened in 99 yeast strains isolated from the nests of the leaf-cutting ant Atta sexdens against 6 standard sensitive strains, as well as against each other. Among this yeast community killer activity was widespread since 77 strains (78 %) were able to kill or inhibit the growth of at least one standard strain or nest strain. Toxin production was observed in representatives of all the studied genera including Aureobasidium, Rhodotorula, Tremella and Trichosporon, whose killer activity has not yet been described

Fungal Communities In The Garden Chamber Soils Of Leaf-cutting Ants

Leaf-cutting ants modify the properties of the soil adjacent to their nests. Here, we examined whether such an ant-altered environment impacts the belowground fungal communities. Fungal diversity and community structure of soil from the fungus garden chambers of Atta sexdens rubropilosa and Atta bisphaerica, two widespread leaf-cutting ants in Brazil, were determined and compared with non-nest soils. Culture-dependent methods revealed similar species richness but different community compositions between both types of soils. Penicillium janthinellum and Trichoderma spirale were the prevalent isolates in fungus chamber soils and non-nest soils, respectively. In contrast to cultivation methods, analyses of clone libraries based on the internal transcribed spacer (ITS) region indicated that richness of operational taxonomic units significantly differed between soils of the fungus chamber and non-nest soils. FastUnifrac analyses based on ITS sequences further revealed a clear distinction in the community structure between both types of soils. Plectania milleri and an uncultured Clavariaceae fungus were prevalent in fungus chamber soils and non-nest soils, respectively. FastUnifrac analyses also revealed that fungal community structures of soil from the garden chambers markedly differed among ant species. Our findings suggest that leaf-cutting ants affect fungal communities in the soil from the fungus chamber in comparison to non-nest soils.541111861196Schultz, T.R., Brady, S.G., Major evolutionary transitions in ant agriculture (2008) Proc. Natl. Acad. Sci. USA, 105, pp. 5435-5440Weber, N.A., (1972) Gardening Ants: The Attines, , Memoirs of the American Philosophical Society, PhiladelphiaCaldera, E.J., Poulsen, M., Suen, G., Currie, C.R., Insect symbioses: a case study of past, present, and future fungus-growing ant research (2009) Environ. Entomol., 38, pp. 78-92Currie, C.R., Mueller, U.G., Malloch, D., The agricultural pathology of ant fungus gardens (1999) Proc. Natl. Acad. Sci. USA, 96, pp. 7998-8002Currie, C.R., Prevalence and impact of a virulent parasite on a tripartite mutualism (2001) Oecologia, 128, pp. 99-106Mueller, U.G., Symbiont recruitment versus ant-symbiont co-evolution in the attine ant-microbe symbiosys (2012) Curr. Opin. Microbiol., 15, pp. 269-277Little, A.E.F., Currie, C.R., Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis (2007) Biol. Lett., 3, pp. 501-504Little, A.E.F., Currie, C.R., Black yeasts symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants (2008) Ecology, 89, pp. 1216-1222Bacci, M., Jr., Ribeiro, S.B., Casarotto, M.E.F., Pagnocca, F.C., Biopolymer-degrading bacteria from nests of the leaf-cutting ant Atta sexdens rubropilosa (1995) Braz. J. Med. Biol. Res., 28, pp. 79-82Scott, J.J., Budsberg, K.J., Suen, G., Wixon, D.L., Microbial community structure of leaf-cutter ant fungus-gardens and refuse dumps (2010) PLoS ONE, 5, p. e9992Rodrigues, A., Bacci, M., Jr., Mueller, U.G., Ortiz, A., Microfungal "weeds" in the leafcutter ant symbiosis (2008) Microb. Ecol., 56, pp. 604-614Rodrigues, A., Mueller, U.G., Ishak, H.D., Bacci, M., Jr., Ecology of microfungal communities in gardens of fungus-growing ants (Hymenoptera: Formicidae): a year-long survey of three species in Central Texas (2011) FEMS Microbiol. Ecol., 78, pp. 244-255Pinto-Tomás, A.A., Anderson, M.A., Suen, G., Stevenson, D.M., Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants (2009) Science, 326, pp. 1120-1123Currie, C.R., Stuart, A.E., Weeding and grooming of pathogens in agriculture by ants (2001) Proc. R. Soc. B., 268, pp. 1033-1039Cremer, S., Armitage, S.A.O., Schmid-Hempel, P., Social immunity (2007) Curr. Biol., 17, pp. 693-702Vander Meer, R., Ant interactions with soil organisms and associated semiochemicals (2012) J. Chem. Ecol., 38, pp. 728-745Schoenian, I., Spiteller, M., Ghaste, M., Wirth, R., Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants (2011) Proc. Natl. Acad. Sci. USA, 108, pp. 1955-1960Fernández-Marín, H., Zimmerman, J.K., Rehner, S.A., Wcislo, W.T., Active use of the metapleural glands by ants in controlling fungal infection (2006) Proc. R. Soc. B, 273, pp. 1689-1695Fernández-Marín, H., Zimmerman, J.K., Nash, D., Boomsma, J.J., Reduced biological control and enhanced chemical pest management in the evolution of fungus farming ants (2009) Proc. R. Soc. B, 276, pp. 2263-2269Farji-Brener, A.G., Leaf-cutting ant nests and soil biota abundance in a semi-arid steppe of northwestern Patagonia (2010) Sociobiology, 56, pp. 549-557Mora, P., Miambi, E., Jiménez, J.J., Decaëns, T., Functional complement of biogenic structures produced by earthworms, termites and ants in the neotropical savannas (2005) Soil Biol. Biochem., 37, pp. 1043-1048Holec, M., Frouz, J., The effect of two ant species Lasius niger and Lasius flavus on soil properties in two contrasting habitats (2006) Eur. J. Soil Biol., 42, pp. S213-S217Ba, A.S., Phillips, S.A., Anderson, J.T., Yeasts in mound soil of the red imported fire ant (2000) Mycol. Res., 104, pp. 969-973Baird, R., Woolfolk, S., Watson, C.E., Survey of bacterial associates of black/hybrid imported fire ants from mounds in Mississippi (2007) Southeast Natl., 6, pp. 615-632Zettler, J.A., McInnis, T.M., Allen, C.R., Spira, T.P., Biodiversity of fungi in red imported fire ant (Hymenoptera: Formicidae) mounds (2002) Ann. Entomol. Soc. Am., 95, pp. 487-491Folgarait, P., Ant biodiversity and its relationship to ecosystem functioning: a review (1998) Biodivers. Conserv., 7, pp. 1221-1244Hudson, T.M., Turner, B.L., Herz, H., Robinson, J.S., Temporal patterns of nutrient availability around nests of leaf-cutting ants (Atta colombica) in secondary moist tropical forest (2009) Soil Biol. Biochem., 41, pp. 1088-1093Jones, C.G., Lawton, J.H., Shachak, M., Organisms as ecosystem engineers (1994) Oikos, 69, pp. 373-386Jiménez, J.J., Decaëns, T., Chemical variations in the biostructures produced by soil ecosystem engineers. Examples from the neotropical savannas (2006) Eur. J. Soil Biol., 42, pp. S92-S102Jiménez, J.J., Decaëns, T., Lavelle, P., C and N concentrations in biogenic structures of a soil-feeding termite and a fungus-growing ant in the Colombian savannas (2008) Appl. Soil Ecol., 40, pp. 120-128Moutinho, P., Nepstad, D.C., Davidson, E.A., Influence of leaf-cutting ant nests on secondary forest growth and soil properties in Amazonia (2003) Ecology, 84, pp. 1265-1276Boulton, A.M., Jaffee, B.A., Scow, K.M., Effects of a common harvester ant (Messor andrei) on richness and abundance of soil biota (2003) Appl. Soil Ecol., 23, pp. 257-265Boulton, A.M., Amberman, K.D., How ants increase soil biota richness and abundance: a field experiment (2006) Biodivers. Conserv., 15, pp. 69-82Dauber, J., Niechoj, R., Baltruschat, H., Wolters, V., Soil engineering ants increase grass root arbuscular mycorrhizal colonization (2008) Biol. Fertil. Soils, 44, pp. 791-796Ginzburg, O., Whitford, W.G., Steinberger, Y., Effects of harvester ant (Messor spp.) activity on soil properties and microbial communities in a Negev Desert ecosystem (2008) Biol. Fertil. Soils, 45, pp. 165-173Ishak, H.D., Plowes, R., Sen, R., Kellner, K., Bacterial diversity in Solenopsis invicta and Solenopsis geminata ant colonies characterized by 16S amplicon 454 pyrosequencing (2011) Env. Microbiol., 61, pp. 821-831Dauber, J., Wolters, V., Microbial activity and functional diversity in the mounds of the three different ant species (2000) Soil. Biol. Biochem., 32, pp. 93-99Moreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae) nests (2004) J. Appl. Entomol., 128, pp. 204-211Rodrigues, A., Cable, R.N., Mueller, U.G., Bacci, M., Jr., Antagonistic interaction between garden yeasts and microfungal garden pathogens of leaf-cutting ants (2009) Anton. van Leeuwen., 96, pp. 331-342Domsch, K.H., Gams, W., Anderson, T., (1980) Compendium of Soil Fungi, , Academic Press, LondonSamson, R.A., Hoekstra, E.S., Frisvad, J.C., (2000) Introduction to Food-Airborne Fungi, , 6th edn., Centraalbureau voor Schimmelcultures, BaarnKlich, M.A., (2002) Identification of common Aspergillus species, , Centraalbureau voor Schimmelcultures, BaarnPitt, J.I., (2000) A Laboratory Guide to Common Penicillium Species, , 3rd edn., Commonwealth Scientific and Industrial Research Organization, North RydeSampaio, J.P., Gadanho, M., Santos, S., Duarte, F.L., Polyphasic taxonomy of the basidiomycetous yeast genus Rhodosporidium: Rhodosporidium kratochvilovae and related anamorphic species (2001) Int. J. Syst. Evol. 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Low variation in ribosomal DNA and internal transcribed spacers of the symbiotic fungi of leaf-cutting ants (Attini: Formicidae)

Leaf-cutting ants of the genera Atta and Acromyrmex (tribe Attini) are symbiotic with basidiomycete fungi of the genus Leucoagaricus (tribe Leucocoprineae), which they cultivate on vegetable matter inside their nests. We determined the variation of the 28S, 18S, and 5.8S ribosomal DNA (rDNA) gene loci and the rapidly evolving internal transcribed spacers 1 and 2 (ITS1 and ITS2) of 15 sympatric and allopatric fungi associated with colonies of 11 species of leafcutter ants living up to 2,600 km apart in Brazil. We found that the fungal rDNA and ITS sequences from different species of ants were identical (or nearly identical) to each other, whereas 10 GenBank Leucoagaricus species showed higher ITS variation. Our findings suggest that Atta and Acromyrmex leafcutters living in geographic sites that are very distant from each other cultivate a single fungal species made up of closely related lineages of Leucoagaricus gongylophorus. We discuss the strikingly high similarity in the ITS1 and ITS2 regions of the Atta and Acromyrmex symbiotic L. gongylophorus studied by us, in contrast to the lower similarity displayed by their non-symbiotic counterparts. We suggest that the similarity of our L. gongylophorus isolates is an indication of the recent association of the fungus with these ants, and propose that both the intense lateral transmission of fungal material within leafcutter nests and the selection of more adapted fungal strains are involved in the homogenization of the symbiotic fungal stock

Taxonomic Assessment And Enzymes Production By Yeasts Isolated From Marine And Terrestrial Antarctic Samples

The aim of the present study was to investigate the taxonomic identity of yeasts isolated from the Antarctic continent and to evaluate their ability to produce enzymes (lipase, protease and xylanase) at low and moderate temperatures. A total of 97 yeast strains were recovered from marine and terrestrial samples collected in the Antarctica. The highest amount of yeast strains was obtained from marine sediments, followed by lichens, ornithogenic soils, sea stars, Salpa sp., algae, sea urchin, sea squirt, stone with lichens, Nacella concinna, sea sponge, sea isopod and sea snail. Data from polyphasic taxonomy revealed the presence of 21 yeast species, distributed in the phylum Ascomycota (n = 8) and Basidiomycota (n = 13). Representatives of encapsulated yeasts, belonging to genera Rhodotorula and Cryptococcus were recovered from 7 different Antarctic samples. Moreover, Candida glaebosa, Cryptococcus victoriae, Meyerozyma (Pichia) guilliermondii, Rhodotorula mucilaginosa and R. laryngis were the most abundant yeast species recovered. This is the first report of the occurrence of some species of yeasts recovered from Antarctic marine invertebrates. Additionally, results from enzymes production at low/moderate temperatures revealed that the Antarctic environment contains metabolically diverse cultivable yeasts, which could be considered as a target for biotechnological applications. Among the evaluated yeasts in the present study 46.39, 37.11 and 14.43 % were able to produce lipase (at 15 °C), xylanase (at 15 °C) and protease (at 25 °C), respectively. The majority of lipolytic, proteolytic and xylanolytic strains were distributed in the phylum Basidiomycota and were mainly recovered from sea stars, lichens, sea urchin and marine sediments. © 2013 Springer Japan.17610231035Almeida, J.M.G.C.F., Yeast community survey in the Tagus estuary (2005) FEMS Microbiol Ecol, 53, pp. 295-303Arenz, B.E., Blanchette, R.A., Distribution and abundance of soil fungi in Antarctica at sites on the Peninsula, Ross Sea Region and McMurdo Dry Valleys (2010) Soil Biol Biochem, 43, pp. 308-315Bölter, M., Kandeler, E., Pietr, S.J., Seppelt, R.D., Heterotrophic Microbes, Microbial and Enzymatic Activity in Antarctic Soils (2002) Geoecol Antarct Ice-Free Coast Landsc Ecol Stud, 154, pp. 189-214Bon, E.P., Costa, R.B., Silva, M.V.A., Leitao, V.S.F., Freitas, S.P., Ferrara, M.A., Mercado e Perspectivas de Uso de Enzimas Industriais e Especiais no Brasil (2008) Interciência, Rio De Janeiro, 20, pp. 463-488. , In: Enzimas em Biotecnologia- Produção, Aplicações e Mercado, EdBurgaud, G., Arzur, D., Durand, L., Cambon-Bonavita, M., Barbier, G., Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna (2010) FEMS Microbiol Ecol, 73, pp. 121-133Carrasco, M., Rozas, J.M., Barahona, S., Alcaíno, J., Cifuentes, V., Baeza, M., Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region (2012) BMC Microbiol, 12, p. 251Charoenchai, C., Fleet, G.H., Henschke, P.A., Todd, B., Screening of non-Saccharomyces wine yeasts for the presence of extracellular hydrolytic enzymes (1997) Aust J Grape Wine Res, 3, pp. 2-8Connell, L., Redman, R., Craig, S., Scorzetti, G., Iszard, M., Rodriguez, R., Diversity of soil yeasts isolated from South Victoria Land, Antarctica (2008) Microbiol Ecol, 56, pp. 448-459Crowe, J.H., Crowe, L.M., Carpenter, J.F., Wistrom, C.A., Stabilization of dry phospholipid bilayers and proteins by sugars (1987) Biochem J, 242, pp. 1-10Crowe, J.H., Hoekstra, F.A., Crowe, L.M., Anhydrobiosis (1992) Annu Rev Physiol, 54, pp. 579-599Feller, G., Gerday, C., Psychrophilic enzymes: hot topics in cold adaptation (2003) Nat Rev Microbiol, 1, pp. 200-208Frisvad, J.C., Fungi in cold ecosystems (2008) Psychrophiles: From Biodiversity to Biotechnology, pp. 137-156. , R. 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Gerday (Eds.), Berlin: SpringerGadanho, M., Sampaio, J.P., Cryptococcus ibericus sp. nov., Cryptococcus aciditolerans sp. nov. and Cryptococcus metallitolerans sp. nov., a new ecoclade of anamorphic basidiomycetous yeast species from an extreme environment associated with acid rock drainage in São Domingos pyrite mine, Portugal (2009) Int J Syst Evol Microbiol, 59, pp. 2375-2379Geok, L.P., Razak, C.A.N., Rahman, R.N.Z.A., Basri, M., Salleh, A.B., Isolation and screening of an extracellular organic solvent-tolerant protease producer (2003) Biochem Eng J, 13, pp. 73-77Gomes, J., Gomes, I., Steiner, W., Thermolabile xylanase of the Antarctic yeast Cryptococcus adeliae: production and properties (2000) Extremophiles, 4, pp. 227-235Hall, T.A., Bio Edit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/ 98/NT (1999) Nucl Acids Symp Ser, 41, pp. 95-98Joseph, B., Ramteke, P.W., Thomas, G., Cold active microbial lipases: some hot issues and recent developments (2008) Biotechnol Adv, 26, pp. 457-470Knob, A., Carmona, E.C., Xylanase production by Penicillium sclerotiorum and its characterization (2008) World Appl Sci J, 4 (2), pp. 277-283Kohlmeyer, J., Kohlmeyer, E., (1979) Marine Micology: The Higher Fungi, , New York: Academic PressKouker, G., Jaeger, K.E., Specific and sensitive plate assay for bacterial lipases (1987) Appl Environ Microbiol, 53, pp. 211-213Kurtzman, C.P., Fell, J.W., Boekhout, T., Robert, V., Methods for isolation, phenotypic characterization and maintenance of yeasts (2011) The Yeasts: A Taxonomic Study, pp. 88-110. , 5th edn., C. 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Low variation in ribosomal DNA and internal transcribed spacers of the symbiotic fungi of leaf-cutting ants (Attini: Formicidae)

Leaf-cutting ants of the genera Atta and Acromyrmex (tribe Attini) are symbiotic with basidiomycete fungi of the genus Leucoagaricus (tribe Leucocoprineae), which they cultivate on vegetable matter inside their nests. We determined the variation of the 28S, 18S, and 5.8S ribosomal DNA (rDNA) gene loci and the rapidly evolving internal transcribed spacers 1 and 2 (ITS1 and ITS2) of 15 sympatric and allopatric fungi associated with colonies of 11 species of leafcutter ants living up to 2,600 km apart in Brazil. We found that the fungal rDNA and ITS sequences from different species of ants were identical (or nearly identical) to each other, whereas 10 GenBank Leucoagaricus species showed higher ITS variation. Our findings suggest that Atta and Acromyrmex leafcutters living in geographic sites that are very distant from each other cultivate a single fungal species made up of closely related lineages of Leucoagaricus gongylophorus. We discuss the strikingly high similarity in the ITS1 and ITS2 regions of the Atta and Acromyrmex symbiotic L. gongylophorus studied by us, in contrast to the lower similarity displayed by their non-symbiotic counterparts. We suggest that the similarity of our L. gongylophorus isolates is an indication of the recent association of the fungus with these ants, and propose that both the intense lateral transmission of fungal material within leafcutter nests and the selection of more adapted fungal strains are involved in the homogenization of the symbiotic fungal stock