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ISSN 19950829, Inland Water Biology, 2014, Vol. 7, No. 4, pp. 352–356. © Pleiades Publishing, Ltd., 2014.

AQUATIC MYCOLOGY

Terrigenous Micromycetes in Freshwater (Review) L. V. Voronin Ushinsky State Pedagogical University, Yaroslavl, Russia email: [email protected] Received July 17, 2013

Abstract—The occurrence, , and taxonomical composition of fungi have been analyzed for differ ent compounds of the freshwater ecosystems of various natural zones (from tundra to desert), particularly, for , , on living and dead plant substrates, and on some species. The role of terrigenous fungi in the freshwater ecosystems is discussed.

Keywords: , phylloplane fungi, mycobiota of fish, decomposing fungi, terrigenous micro mycetes, ascomycetes, mitosporic fungi, freshwater ecosystems DOI: 10.1134/S1995082914040191

Fungi are indispensable components of the biota of and water reservoirs [13, 41]. In most cases, the mini any . The aquatic mycobiota includes mal abundance of the spores of the terrestrial fungi is numerous species belonging to various ecological and in the middle water layer and the maximal is in the taxonomical groups. True aquatic fungi (chytridio nearbottom water layer, where they accumulate dur mycetes) and fungilike organisms () are res ing sedimentation [43]. The abundance of diaspores of idents of the aquatic environment; their lifecycle these fungi increases after rainfall and stays high for occurs in the water. Secondary aquatic fungi are several days after. Spores of Mucor and Penicillium another group, including mostly aquatic hypho dominate in the Lake District in England [27]. These mycetes inhabiting and rivers; their whole life spores and the spores of the other terrestrial fungi swell cycle also takes place in the water. This group also and sink to the bottom. As a result, the spores of Mucor comprises the aquatic ascomycetes inhabiting lotic fungi dominate on the surface of the silts; these spores and lentic waters. Air–aquatic (amphibian) hypho can stay alive even when the oxygen supply is limited. mycetes are the third group. They develop on sub The spores of Penicillium genus are hydrophobic; they merged substrates but form spores only if the substrate swell slowly and stay in the neiston and plankton has been exposed to the air. Some ascomycetes are longer [27]. Some spores are utilized by bacteria [20]; probably also thus defined. The fungi of all three however, the spores of many soil fungi may stay alive in groups relate closely to the aquatic environment. the water for a long time period, and survivability Terrestrial micromycetes are a separate group; increases when the concentrations of nitrates and these fungi belong to different taxonomical groups and phosphorus in the water are high [1, 2]. Therefore, the are characterized by differing biology. They penetrate spores of the soil fungi, especially of genera Fusarium the aquatic environment by different pathways. Some and Penicillium, may become a significant component of them come as spores and fragments of mycelia with of the plankton and benthos in the eutrophicated the air and soil particles, dead organic, etc. Micro waterbodies [3, 4, 24]. They may serve as a food source mycetes develop on the leaves of all terrestrial trees for [14]. The spores of some micro and bushes; they utilize plant metabolites and enter mycetes may germinate at different depths and in the the water on falling leaves. bottom sediments, as was observed for Cladosporium The diaspores (propagules or other fungi germs of and Penicillium genera [27], and found experimentally different genesis) of the terrestrial fungi are usually for Alternaria alternate (Fr.) Keissl. and Fusarium sp. found when studying the aquatic environment; how [22, 23]. In the bottom sediments, the of ever, the and their role in the ecosys mycelia may reach up to 88% of the total fungal biom tem still receive less attention. This study reviews data ass (as was found by the method of bioluminescent on terrigenous micromycetes and their role in the microscopy), which may evidence the activity of the freshwater environment. terrestrial micromycetes in the aquatic environment [25]. Yeastlike fungi Aureobasidium pullulans (dBy.) Arnaud are considered temporary or even perma Micromycetes in the Plankton and Benthos nently active in the aquatic environment. The The propagules of zygomycetes and, frequently, the propagules of dozens of terrestrial fungi species were mitosporic fungi, are found in streams, rivers, lakes, registered in the mycobiota of the bottom sediments of

352 TERRIGENOUS MICROMYCETES IN FRESHWATER ECOSYSTEMS 353 the lakes and other standing; these fungi species are or as a food source for , or they may col common for the terrestrial environment of different onize organic substrates and destroy them [14]. climatic zones, where mitosporic hyphomycetes dom The abundance of the fungi propagules in the water inate [18, 22, 23, 38, 39, 42]. column and bottom sediments increases together with Sedentary benthic organisms frequently carry ther the lake , but the species diversity mophilic terrestrial zygomycetes, ascomycetes, and decreases [10, 11, 28, 29, 34–37]. For example, the hyphomycetes [31, 48, 49]. The possibility of develop spore abundance varies from 2000 spores per liter in ment of some fungi in the benthic species cannot be oligo–mesotrophic Celije Lake up to 4900 spores per excluded, especially if the waterbody receives the load. liter in eutrophic Gruzha Lake [43]. In hyper For example, hyphomycete Acremonium kiliense eutrophic Tilsi Pikkjarv (Estonia), the fungi diaspore W. Gams was registered at the gills and in the intestine abundance was 1100 spores/L in the surface water layer of mollusk Dreissena polymorpha sampled at Shoshin and 2900 spores/L in the bottom water layer [10]. In skii Ples of Ivan’kovskoe Reservoir [21]. eutrophic lakes of western Latvia, the fungi diaspore abundance reaches 34.400 spores/L and the dominat The diaspores of the terrestrial fungi are intensively ing genera are Fusarium, Penicillium, Aspergillus, Cla transported with the rain outflow. The rivers inflowing dosporium, Mucor, and Rhizopus [15]. the lakes bring much of this material. For example, in The load of waterbodies from household, agricul the of Trubezh River (Pleshcheevo Lake), the tural, and industrial waste has a significant effect on high abundance of fungi diaspores has been observed the mycobiota of aquatic ecosystems. A similar pattern all year round regardless of season, but decreasing is observed in both lotic and lentic waters [22–24]. from the estuary to the lake center 10–100 times [18]. Fungi diversity decreases because of the disappearance Two seasonal peaks of mitosporic micromycetes, of species sensitive to particular pollutants, but the and autumn, are observed in the lakes [18, 34, total abundance may remain the same or even increase 35, 42, 47]. In Pleshcheevo Lake, the first peak occurs because of the active growth of the tolerant species in March–May and the second occurs in September– [22, 23, 30, 32]. Dermatophytes and other keratino November. During these periods, the abundance of philic fungi occur in up to 76.6% of the samples of the the diaspores of micromycetes increases more than bottom sediments [26, 50–52]. Such restructuring of tenfold and may reach hundreds of thousands per liter the micromycete complex is not endless, since the [18]. If the trophic status of the lake is high, the sea growth of most of the fungi stops at a high pollution sonal dynamics are less pronounced, as is observed level and their abundance decreases [45, 46]. When during the comparison of the mycoplankton of studying the mycobiota of Vasilievskie Lakes (the mesotrophic Pyashechno Lake and eutrophic Gle urban area of the city of Tolyatti) polluted by house bokoe Lake in Poland [35]. The autumn peak of the hold waste [22, 23], darkpigmented micromycetes abundance of the fungi propagules is preconditioned dominate; these fungi are the most tolerant to unfa by their transport with the and soil particles vorable anthropogenic load, but the abundance of coming from the watershed areas, especially after rain, micromycetes in highly polluted waterbodies is low. as well as with the transport by the leaf fall and autoch Such a reaction of mycobiota on the pollution must be thonous organic matter [42], supported by the maxi taken into account when assessing the ecological sta mal abundance of micromycete propagules in the sur tus of the aquatic environment [24]. face water layer [18]. The spring peak of the fungi abundance links to an increase in the autochthonous food sources for the fungi, i.e., with the death of dia Micromycetes–Phylloplanes of Hydrophytes toms after the [42]. In Loch Ness they Phylloplane fungi inhabit the leaf surface and use are considered an endogenous active population of the metabolites of the plants (amino acids, carbohydrates, yeast belonging to the terrestrial fungi [42]. The popu auxins, and other compounds) as a food source. They lation of the mycelia fungi forms predominantly in the refer to a specific ecological group. The phylloplane coastal zone and has periodic or sporadic activity, mycobiota of Nuphar lutea (L.) Smith has been stud which is pronounced mostly in spring. During the ied in six lakes of Darwin Nature Reserve and in six same period, the active growth of facultative aquatic lakes of VerkheSudskie lake system in Vologda oblast (originally, terrestrial) micromycetes takes place in the [13]. The leaves of yellow water lilies are colonized by bottom sediments, supported by the insignificant the fungi before they open. The yeasts and mycelia income of the allochthonous organic matter to the fungi colonize the leaves gradually; the maximal abun lake in comparison to large income during the autumn dance is observed in June and stays through the sum [42]. Generally, the question about the activity of the mer. The distribution of many yeast species in the terrestrial micromycetes in the aquatic environment water and submerged substrates, as well as their growth remains open. Despite that, we suppose that the ter in the liquid media, is wellknown, so we have focused restrial fungi at the stage of propagule may pass here on the mycelia phylloplane fungi. These fungi through a different without any form the complexes on the upper and lower side of the effect, they may serve as a substrate for the microfauna leaves of yellow water lily, and their abundance is usu

INLAND WATER BIOLOGY Vol. 7 No. 4 2014 354 VORONIN ally higher on the upper side [13]. Therefore, the ence of terrestrial fungi on aquatic substrates [13, 17, aquatic environment limits the distribution of these 33, 34, 37, 41, 44, 53]. First and foremost, these are fungi, since exclusively terrestrial micromycetes have phylloplane fungi of both hydrophytes and fallen been found in such complexes. leaves in the aquatic environment. The abundance of The number of phylloplane fungi of the yellow these fungi in such environment decreases dramati waterlily complex is not high, from 3 to 9 species, but cally; however, some strains develop on the substrates it stays relatively stable. In the meantime, the ratio of until the water temperature decreases and becomes a the species composition changes when the dominating limiting factor [13, 33]. Some terrestrial micromycetes species may alter and the species may appear or disap may be active on the plant substrates in the aquatic pear in the complex. For example, the abundance of environment, but they cannot compete with destruct Cladosporium genus increases from May through July, ing prokaryotes [53]. The role of bacteria and fungi in and two or three species dominate in June (C. cladospo the destruction of the plant substrates and their rela rioides (Fres.) de Vries, C. herbarum (Pers.) Link, and tionships are still unknown; these processes depend on C. avellaneum de Vries), but the only C. herbarum dom the biology of these organisms and on the type and ori inates in July [13]. In all the acid lakes of the Darwin gin of substrate and the type of waterbody [17]. Nature Reserve (Motykino, Zmeinoe, Dubrovskoe), Special attention must be paid to the group of vari the abundance of Hormonema dematioides Lagerb. et ous mitosporic ascomycetes that may be active in the Melin is higher than in the neutral Khotavets Lake and aquatic environment and that refer to the “immigrants” in acescent Krivoe Lake. Therefore, our results on according to the Park classification [40]; i.e., they can developing and maintaining the phylloplane myco be met in both aquatic and air environments. They biota complexes do not contradict the theory of the comprise the genera Acrodictys, Acrogenospora, Arthro island of McArthur [13]. Such com botrys, Bactrodesmium, Brachysporiella, Cordana, Dic plexes are characterized by the dynamic equilibrium of tyosporium, Ellisembia, Spadicoides, Sporidesmiella, the species number maintained by the processes of and Trichocladium [44]. immigration and disappearance of the species from the complex, followed by the naturalization of tolerant and eurybiont species [12]. Normal Mycobiota of the Fish The coefficients of similarity of the species compo The studies of normal (nonpathogenic) mycobiota sition of mycobiota of the upper and lower leaf sides, of different species (bream, pikeperch, in regard to the seasonal dynamics, evidence different pike, roach, etc.) in waterbodies of different types migration pathways of propagules that affect the devel located in various geographic zones (Volga River reser opment of the fungi complex. The stabilization of the voirs, Danube , Ladoga Lake, Balkhash fungi composition on the lower (submerged) leaf side Lake, IssykKul Lake, etc.) evidenced the nonspecific takes more time, which probably links to the flushing saprotrophic fungi species associated with ichthyo of the propagules, especially during the wind mixing, fauna [5–8]. The fungi complexes located on fish and obstacles for their anchoring, so the free space for organs exposed to the external environment (body sur colonizing exist for a longer time period. In the middle face, gills, and gut content) are presented by terrestrial of the vegetation period, the “aligning” of the fungi species. The spore abundance depends on the loca complexes finishes on both sides of the leaf; i.e., the tion; i.e., from 4.3 ± 0.8 to 57.8 ± 7.0 CFC per 1 cm2 limiting factor of the substrate (metabolites) is clearly are found on the body surface, 2.2 ± 0.4–27.2 ± seen for the eccrisotrophic fungi. This is also sup 4.7 CFC per one gram of the gills, and 2.5 ± 0.8– ported by the increase in the coefficient of the species 18.8 ± 2.6 CFC per one gram of the gut content [5, 7]. similarity of Soerensen–Chekanovsky calculated for The composition of the dominant and most common the phylloplane mycobiota of yellow water lily sam fungi species is relatively stable and includes several pled at different lakes, when this coefficient ranged taxa: Phoma glomerata (Cda.) Wr. et Hjchapf., from 40–61% in June to 67–76%, in July. In general, Ph. eupyrena Sacc., Ph. medicaginis Malbr. et Roum. 61 species of the terrestrial fungi of 28 genera have var. pinodella (L.K. Jones) Boerema, Ph. herbarum been registered in the phylloplane mycobiota of yellow West., different Penicillium species, Mucor circinelloides water lily of the small lakes of Vologda oblast [13]. v. Ti e g h . , M. hiemalis Wehmer, Trichoderma viride Pers. ex S.F. Grey, and T. koningii Oud. In total, 147 fungi species and subspecies have been registered, and about Fungi Destructing the Plant Substrates 140 of them are in the terrestrial group [6, 7]. The role of the fungi participating in destruction of The fungi complex on the fish depends on the type the plant substrates in the aquatic environment has of waterbody. The fish inhabiting oligotrophic water been studied poorly. When addressing this issue, the bodies carry Penicillium, Mucor, and Rhizopus; those only impact of the aquatic hyphomycetes (in the lakes in distrophic ones carry Penicillium and Mortierella; and rivers) or aquatic ascomycetes and air–aquatic and species variability is the highest in the meso and hyphomycetes (in lentic and slowlotic waterbodies) is eutrophic environment, where species of Phoma, Pen considered. However, many authors indicate the pres icillium, Mucor, Rhizopus, Trichoderma, Cladospo

INLAND WATER BIOLOGY Vol. 7 No. 4 2014 TERRIGENOUS MICROMYCETES IN FRESHWATER ECOSYSTEMS 355 rium, Alternaria, Fusarium, Aureobasidium, and some 5. Voronin, L.V., Mycoflora of fish of the Danube Delta, others have been registered [5, 7]. Mikol. Fitopatol., 1984, vol. 18, no. 4, pp. 265–270. Terrestrial fungi stay on the fish permanently and 6. Voronin, L.V., Fungi developing on the bream and form complexes. A significant spring maximum and pikeperch of some freshwater bodies, Mikol. Fitopatol., less pronounced autumn maximum of the fungi spore 1986, vol. 20, no. 5, pp. 353–361. 7. Voronin, L.V., Mycoflora of some fish species of the abundance have been observed for the bream in Kuibyshev Reservoir, in Biologiya vnutrennikh vod: Rybinsk Reservoir; these maxima coincided with Inform. Byul. (Inland Water Biology: Inform. Bulletin), peaks of fungi diaspore abundance in the water and Leningrad, 1987, vol. 76, pp. 11–15. followed the frequency of occurrence and ratio of a 8. Voronin, L.V., Seasonal changes in the mycobiota of the particular species within the season [8]. bream in the Rybinsk Mikol. Fitopatol., 1987, vol. 21, The morphophysiological status of the terrestrial no. 5, pp. 409–415. fungi located on the fish is very important, i.e., 9. Voronin, L.V., The main groups of saprotrophic fungi whether they are active or presented by the hibernating on the pike body surface, in Biologiya vnutrennikh vod: structures. It was found experimentally that the myco Inform. Byul. (Inland Water Biology: Inform. Bulletin), Leningrad, 1989, vol. 83, pp. 16–19. biota of the fish body surface was presented by two 10. Voronin, L.V., Saprotrophic fungi of lakes of Estonia. 2. fungi groups: spores (diapausing structures) and Abundance and distribution of fungi in halotrophic, actively growing mycelia in the mucus [9]. The spores hypereutrophic, and mesotrophic lakes, in Biologiya probably attach to the fish body, and their number vnutrennikh vod: Inform. byul (Inland Water Biology: depends directly on their concentration in the water. Inform. Bulletin), Leningrad, 1991, vol. 90, pp. 11–15. The mycelia of Phoma and Cladosporium use the fish as 11. Voronin, L.V., Mycological indication of the state of a substrate, and their diaspores are characterized by ecosystems of water bodies of Vorkuta and its environs, the selectivity. We suppose that the fungi developing on in Bioindikatsiya sostoyaniya prirodnoi sredy Vorkutin the fish body surface belong to commensal species. skoi tundry (Bioindication of the State of the Environ However, the parasitic relationships may not be ment of the Vorkuta Tundra), Syktyvkar: Komi Nauch. excluded for some of them. Experimental studies Tsentr UrO RAN, 1996, pp. 83–91. 12. Voronin, L.V., Phylloplane fungi Nuphar lutea (L.) allowed us to define a different level of pathogenic Smith in small rivers of the Rybinsk Reservoir, Yaroslav. potential of the strains of fungi species Phoma glomer Ped. Vestn., 2010, no. 1, pp. 91–95. ata dominating in the fish mycobiota. The pathogenic 13. Voronin, L.V., Mikobiota malykh ozer tundrovoi i lesnoi effect depends on the immune status of the fish; the zon (Mycobiota of Small Lakes of the Tundra and For fungi develop in the intestine wall, splanchnic cavity, est Zones), Yaroslavl: Izd. Yaroslav. Gos. Ped. Univ., and liver [16]. 2010. Since the 1990s, studies of the nonpathogenic 14. Voronin, L.V., Mycobiota of small lakes of the Darwin mycobiota of fish have become very rare in Russia and Reserve, in Rol’ botanicheskikh sadov i okhranyaemykh other countries, and only data on yeast mycobiota and prirodnykh territorii v izuchenii i sokhranenii raznoo braziya rastenii i gribov: Mater. Vseros. nauch. konf. semination of salmon eggs in a fish farm in Ukraine (The Role of Botanic Gardens and Natural Protected exist [19]. Areas in the Study and Conservation of Plant and Fun gal Diversity: Proc. AllRussia Sci. Conf.), Yaroslavl, 2011, pp. 167–170. CONCLUSIONS 15. Voronin, L.V. and Zakharova, L.I., Abundance and The publication review and original studies evi composition of fungi in the lakes of the Latvian SSR dences the significant role of terrestrial micromycetes and Yaroslavl oblast, in Biologiya vnutrennikh vod: in the aquatic environment. The current data are not Inform. Byul. (Inland Water Biology: Inform. Bulletin), enough to assess their role in the structure of the Leningrad, 1988, vol. 78, pp. 11–14. aquatic ecosystems, and future studies must focus on 16. Voronin, L.V. and Mikryakov, V.R., The role of Phoma glomerata (Cda.) Wr. et Hochapfel in fish mycobiota, this important issue. Mikol. Fitopatol., 1992, vol. 26, no. 6, pp. 456–460. 17. 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