Eukaryotic Microbial Communities Associated with Rock-­dwelling Foliose Lichens: A Functional Morphological and Microecological Analysis

Nicholas Bock,

O. Roger Anderson


Lichens are widely recognized as important examples of a fungal-algal or fungal-cyanophyte symbiosis; and in some cases they are a major food source for some animal grazers such as caribou (Rangifer tarandus), especially in the Arctic during winter. However, relatively little is known about the ecology of their co-associated bacterial and protistan communities. This is one of the first reports of an analysis of microbial communities associated with rock-dwelling foliose lichens (Flavoparmelia sp.), including a more detailed analysis of the microbial communities associated with segments of the shield-like, radially arranged lobes. Samples were taken from lichens on granite boulders beneath an oak and maple tree stand on the Lamont-Doherty Earth Observatory Campus, Palisades, N.Y. The bacteria and protist members of the lichen associated microbial communities are comparable to recently reported associations for foliose lichens growing on tree bark at the same locale, including the presence of large myxomycete plasmodial amebas, heterotrophic nanoflagellates, and naked and testate amebas. To obtain evidence of possible differences in the microecology of different portions of each radial lobe, three segments of the radial lobe in the shield-like lichen were sampled: 1) inner, more mature, central segment; 2) middle section linking the central and peripheral segments; and 3) outer, peripheral, usually broader, less closely attached segment. The mean densities (number/g) and biomasses (µg/g) of bacteria and heterotrophic nanoflagellates were highest in the older central segment and lowest in the peripheral segment of the radial lobes, especially when expressed on moist weight basis. Large myxomycete plasmodial amebas were typically located in the outermost segment of the radial lobe. The proportion of vannellid amebas (Vannella spp. and Cochliopodium spp.) were significantly more abundant in the samples of the inner lobes compared to non-vannellid amebas that were more prevalent in the outer lobes. The outer segment of the thallus lobe was typically more spongiose and absorbed more water per unit weight (based on a wet/dry-weight ratio) than the innermost segment. In general, patterns of densities and taxonomic composition of bacteria and eukaryotic microbes intergraded from the inner most segment to the outer part of each lobe – indicating a possible microecological gradient, coincident with the age-related and morphological radial gradations of the lobe. Overall, the evidence shows that the radial variation in the morphology and age-related variables of the three lobe segments may affect the microenvironment of the lobe segments and hence influence the organization of the microbial communities within each segment.

Słowa kluczowe: Algal symbiosis, amebas, bacteria, carbon-biomass, Flavoparmelia, food webs, heterotrophic nanoflagellates, microbial communities

Anderson O. R. (2002) Laboratory and field-based studies of abundances, small-scale patchiness, and diversity of gymnamoebae in soils of varying porosity and organic content: evidence of microbiocoenoses. J. Eukaryot. Microbiol49: 1824

Anderson O. R. (2006) A method for estimating cell volume of amoebae based on measurements of cell length of motile forms: physiological and ecological applications. J. Eukaryot. Microbiol. 53: 185187

Anderson O. R. (2008) The role of amoeboid protists and the microbial community in moss-rich terrestrial ecosystems: biogeochemical implications for the carbon budget and carbon cycle, especially at higher latitudes. J. Eukaryot. Microbiol. 55: 145150

Anderson O. R. (2014) Microbial communities associated with tree bark foliose lichens: a perspective on their microecology. J. Eukaryot. Microbiol. 61: 364–370

Anderson O. R., Gorrell T., Bergen A., Kruzansky R., Levandowsky M. (2001) Naked amoebae and bacteria in an oil impacted salt marsh community. Microb. Ecol42: 474481

Armstrong R. A., Bradwell T. (2011) Growth of foliose lichens: a review. Symbiosis 53: 1–16

Arnold A. E., Miadlikowska J., Higgins K. L., Sarvate S. D., Gugger P., Way A., Hofstetter V., Kauff F., Lutzoni F. (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst. Biol58: 283297

Bates S. T., Cropsey G. W., Caporaso J. B., Knight R., Fierer N. (2011) Bacterial communities associated with the lichen symbiosis. Appl. Environ. Microbiol77: 1309314

Bates S. T., Berg-Lyons D., Lauber C. L., Walters W. A., Knight R., Fierer N. (2012) A preliminary survey of lichen associated eukaryotes using pyrosequencing. Lichenologist 44: 137146

Beyens L., Chardez D., DeLandtsheer R. (1986) Testate amoebae populations from moss and lichen habitats in the Arctic. Polar Biol5: 165174

Berryman S., McCune B. (2006) Estimating epiphytic macrolichen biomass from topography, stand structure and lichen community data. J. Veg. Sci17: 157170

Büdel B., Scheidegger C. (2008) Thallus morphology and anatomy. In: Lichen Biology, (Ed. T. H. Nash III). Cambridge University Press, Cambridge, pp. 40–68

Cardinale M., Puglia A. M., Grube M. (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol. Ecol57: 484495

Cardinale M., Stelnova J., Rabensteiner J., Berg G., Grube M. (2012) Age, sun and substrate: triggers of bacterial communities in lichens. Environ. Microb. Rep4: 2328

Clement J. P., Shaw D. C. (1999) Crown structure and the distribution of epiphyte functional group biomass in oldgrowth Pseudo­tsuga menziesii trees. Ecoscience 6: 243254

de Vries M. C., Watling J. R. (2008) Differences in the utilization of water vapour and free water in two co-occurring foliose lichens from semi-arid southern Australia. Austral. Ecol33: 975–985

Edinger D. C. (2013) An autumn survey of the vascular flora, birds, fungi, myxomycetes and lichens of Baladjie Lake Nature Reserve and Baladjie Rock. West. Austral. Nat26: 126–141

Edwards R. Y. (1960) Quantitative observations on epidendric lichens used as food by caribou. Ecology 41: 425431

Ellis C. J., Crittenden P. D., Scrimgeour C. M., Ashcroft C. J. (2005) Translocation of 15N indicates nitrogen recycling in the mat-forming lichen Cladonia portentosaNew Phytol168: 423–434

Farrar J. F. (1976) The lichen as an ecosystem: observation and experiment. In: Lichenology: Progress and Problems, (Eds. D. H. Brown, D. L. Hawksworth, R. H. Bailey). Academic Press, London, pp. 385406

Gausiaa Y., Palmquist K., Solhaug K. A., Holien H., Hilmo O., Nybakken L., Myhre L. C., Ohlson M. (2007) Growth of epiphytic old forest lichens across climatic and successional gradients. Can. J. Forest Res37: 1832–1845

Grube M., Cardinale M., de Castro J. V. Jr., Müller H., Berg G. (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J3: 1105–1115

Harrisson P. M., Walton D. W. H., Rothery P. (1989) The effects of temperature and moisture on carbon dioxide uptake and total resistance to water loss in the Antarctic foliose lichen Umbilicaria-AntarcticaNew Phytol. 111: 673–682

Hodkinson B. P., Lutzoni F. (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49: 163–180

Honneger R. (1991) Functional aspects of the lichen symbiosis. Ann. Rev. Plant. Phys42: 553–578

Honneger R. (2008) Morphogenesis. In: Lichen Biology, (Ed. T. H. Nash III). Cambridge University Press, Cambridge, 71–95

Honneger R., Peter M., Scherrer S. (1996) Drought-induced structural alterations at the mycobiont-photobiont interface in a range of foliose macrolichens. Protoplasma 190: 221–232

Huiskes A. H. L., Gremmen J. J. M., Francke J. W. (1997) Morphological effects on the water balance of Antarctic foliose and fruticose lichens. Antarct. Sci9: 36–42

Jahns H. M. (1984) Morphology, reproduction and water relations – a system of morphogenetic interactions in Parmelia saxatilisNova Hedwigia 79: 715–737

Johansson O., Palmquist K., Olofsson J. (2012) Nitrogen deposition drives lichen community changes through differential species responses. Global Change Biol18: 2626–2635

Kukwa M. (2005) New or interesting records of lichenicolous fungi from Poland III. Herzogia 18: 37–46

Lawrey J. D., Diederich P. (2003) Lichenicolous fungi: interactions, evolution and biodiversity. Bryologist 106: 80–120

McCune B. (1993) Gradients in epiphyte biomass in three Pseudo­tsuga-Tsuga forests of different ages in western Oregon and Washington. Bryologist 96: 405–411

McCune B., Amsberry K. A., Camacho F. J., Clery S., Cole C., Emerson C., Felder G., French P., Greene D., Harris R., Hutten M., Larson B., Lesko M., Majors S., Markwell T., Parker G. G., Pendergrass K., Peterson E. B., Peterson E. T., Platt J., Proctor J., Rambo T., Rosso A., Shaw D., Turner R., Widmer M. (1997) Vertical profile of epiphytes in a Pacific Northwest old-growth forest. Northwest Sci71: 145–152

Mushegian A. A., Peterson C. N., Baker C. C. M., Pringle A. (2011) Bacterial diversity across individual lichens. Appl. Environ. Microbiol77: 4249–4252

Nash T. H. III (Ed.) (2008a) Lichen Biology. Cambridge: Cambridge University Press

Nash T. H. III (2008b) Introduction. In: Lichen Biology, (Ed. T. H. Nash III). Cambridge University Press, Cambridge, 1–8

Nash T. H. III (2008c) Nitrogen, its metabolism and potential contribution to ecosystems. In: Lichen Biology, (Ed. T. H. Nash III). Cambridge University Press, Cambridge, 184–217

Palmquist K., Dahlman L., Jonsson A., Nash T. H. III (2008) The carbon economy of lichens In: Lichen Biology, (Ed. T. H. Nash III). Cambridge University Press, Cambridge, pp. 218–235

Palmquist K., Dahlman L., Valladares F., Anders T., Sancho L. G., Mattsson J.-E. (2002) CO2 exchange and thallus nitrogen across 75 contrasting lichen associations from different climate zones. Oecologia 133: 295–306

Pelegri S., Dolan J. R., Rassoulzadegan F. (1999) Use of high temperature catalytic oxidation (HTCO) to measure carbon content of microorganisms. Aquat. Microb. Ecol16: 273–280

Pitt C. C. (1927) Succession in lichens. Bryologist 30: 1–4

Roberts D., Zimmer D. (1990) Microfaunal communities associated with epiphytic lichens in Belfast Northern Ireland UK. 
Lichenologist 22: 163–172

Schnittler M., Unterseher M., Pfeiffer T., Novozhilov Y. K., Fiore-Donno A. M. (2010) Ecology of sandstone ravine myxomycetes from Saxonian Switzerland (Germany). Nova Hedwigia 90: 277–302

Seaward M. R. D. (1988) Contribution of lichens to ecosystems. In: CRC Handbook of Lichenology, Vol. 2, (Ed. M. Galun). CRC Press, Boca Raton, 107–129

States J. S., Christensen M., Kinter C. L. (2001) Soil fungi as components of biological soil crusts. In: Biological Soil Crusts: Structure, Function, and Management, (Eds. J. Belnap, O. L. Lange). Springer, New York, 155–166

Thompson J. C. (1958) A preliminary survey of the ciliated Protozoa from treeborne mosses and lichens in the Mountain Lake area. V. J. Sci9: 397

Wilkinson D. M., Creevy A. L., Kalu C. L., Schwartzman D. W. (2014) Are heterotrophic and silica-rich eukaryotic microbes an important part of the lichen symbiosis? MycologyAn International Journal on Fungal Biology, DOI:10.1080/21501203.2014.974084

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