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Geomicrobiology of Eukaryotic Microorganisms Geoffrey M This article was downloaded by: [The University of Manchester Library] On: 16 July 2012, At: 07:43 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Geomicrobiology Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ugmb20 Geomicrobiology of Eukaryotic Microorganisms Geoffrey M. Gadd a & John A. Raven b a Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, Scotland, United Kingdom b Division of Plant Sciences, College of Life Sciences, University of Dundee at SCRI, Scottish Crop Research Institute, Invergowrie, Dundee, Scotland, United Kingdom Version of record first published: 13 Sep 2010 To cite this article: Geoffrey M. Gadd & John A. Raven (2010): Geomicrobiology of Eukaryotic Microorganisms, Geomicrobiology Journal, 27:6-7, 491-519 To link to this article: http://dx.doi.org/10.1080/01490451003703006 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Geomicrobiology Journal, 27:491–519, 2010 Copyright © Taylor & Francis Group, LLC ISSN: 0149-0451 print / 1521-0529 online DOI: 10.1080/01490451003703006 Geomicrobiology of Eukaryotic Microorganisms Geoffrey M. Gadd1 and John A. Raven2 1Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, Scotland, United Kingdom 2Division of Plant Sciences, College of Life Sciences, University of Dundee at SCRI, Scottish Crop Research Institute, Invergowrie, Dundee, Scotland, United Kingdom and organic pollutant degradation. They may also result in adverse Eukaryotic microbes participate in many biogeochemical cy- effects when these processes are associated with the degradation cles, although quantifying their role is not easy, and the discussion of foodstuffs, natural products and building materials, including below comes generally to only qualitative conclusions. Eukary- wood, stone and concrete. otes lack a number of the biogeochemically important functions that are carried out only by archaea (e.g., methanogenesis), bac- Keywords algae, biogeochemical cycles, calcium carbonate, carbon, teria (the anammox chemolithotrophic denitrification reaction), fungi, geomycology, lichens, metalloids, metals, min- or archaea and bacteria (e.g., chemolithotrophy, diazotrophy, and erals, mycorrhizas, phagotrophs, phosphorus, protozoa, dissimilatory reduction of sulfate). Microbial eukaryotes have one saprotrophs, silica ancestral attribute, phagotrophy, which adds a novel link to food webs and thus modifies biogeochemical cycles, and have endosym- bioses as well as ectosymbioses which can recruit metabolism from archaeans (methanogenesis) and bacteria (chemolithotrophic sul- fide oxidation, diazotrophy). The ability of eukaryotes to carry INTRODUCTION out oxidative phosphorylation and the related respiratory car- Eukaryotes have a more restricted range of metabolic bon metabolism, and photosynthesis, as genetically integrated pro- processes encoded in their genomes that have major biogeo- cesses is an outcome of bacterial symbioses. The biogeochemical chemical consequences than do the Archaea and Bacteria importance of fungi is significant in several key areas. These in- clude organic and inorganic transformations, nutrient and ele- (Falkowski et al. 2008; Madigan et al. 2008). Some of these ment cycling, rock and mineral transformations, bioweathering, “deficiencies’ are compensated for by symbioses with Archaea mycogenic mineral formation, fungal-clay interactions, and metal- and, more usually, Bacteria. The extreme of this compensation fungal interactions. Although such transformations can occur in is seen in genetic integration into the eukaryote of the respi- both aquatic and terrestrial habitats, it is in the terrestrial environ- ratory reactions using O as the electron acceptor provided by ment where fungi probably have the greatest influence especially 2 when considering soil, rock and mineral surfaces, and the plant the proteobacterial mitochondrial ancestor, and of the oxygenic root-soil interface. Of special significance are the mutualistic sym- photosynthesis provided by the cyanobacterial plastid ancestor bioses, lichens and mycorrhizas. Geochemical transformations that (Mereschowsky 1905; Kowallik and Martin 1999). Such take place can influence plant productivity and the mobility and endosymbiosis was facilitated by a unique eukaryotic trait, speciation of toxic elements, and are therefore of considerable so- that of the endomembrane and cytoskeletal system permitting cioeconomic relevance. Some fungal transformations have benefi- Downloaded by [The University of Manchester Library] at 07:43 16 July 2012 cial applications in environmental biotechnology, e.g., in metal and phagotrophy and, more generally, endocytosis and exocytosis radionuclide leaching, recovery and detoxification, and xenobiotic and the especially geomicrobiological important possibility of intracellular biomineralization (Cavalier-Smith 1982; Maynard Smith and Szathmary´ 1995). The discussion that follows expands on all these points, Received 7 December 2009; accepted 2 February 2010. encompassing as many eukaryotic microbes and modes of GMG gratefully acknowledges financial support for his own re- search from the Biotechnology and Biological Sciences Research metabolism as possible, and attempting quantitation of the bio- Council, the Natural Environment Research Council, and British Nu- geochemical roles of eukaryotic microbes relative to those of clear Fuels plc. JAR gratefully acknowledges financial support from Archaea and Bacteria (Falkowski et al. 2008), as well as Metazoa the Natural Environment Research Council. The University of Dundee and embryophytic (“higher”) plants. The paper also touches on is a registered Scottish charity No. 015096. the intracellular biomineralization and the possibility of using Address correspondence to Geoffrey M. Gadd, Division of Molecular Microbiology, College of Life Sciences, University of eukaryotic microbes in global bioremediation of anthropogenic Dundee, Dundee, DD1 5EH, Scotland, United Kingdom. E-mail: environmental change, or biogeoengineering. There is particular [email protected] attention paid toward the end of the paper on the role of fungi in 491 492 G. M. GADD AND J. A. RAVEN weathering and decomposition, but also other significant roles benthic habitat also has photosynthetic macroalgae, sometimes of fungi in geomicrobiology. considered with microbes since they are disowned by some plant An important consideration is that the biogeochemical pro- biologists. cesses brought about by eukaryotic microbes do not necessarily Where do photosynthetic eukaryotic microbes fit qualita- directly contribute to the inclusive fitness of the responsible or- tively and quantitatively into the range of organisms with photo- ganisms, but rather are emergent outcomes of natural selection. chemical energy transduction mechanisms, i.e., photosynthetic Examples are some aspects of weathering, and some examples in the broad sense? There are a number of photosynthetic organ- of the extracellular precipitation of particulate minerals that isms among the Archaea and Bacteria. The rhodopsin-catalysed have no obvious skeletal role or modify the external environ- photochemical proton and chloride pumps in many Archaea ment in a way that increases fitness. An additional point is that and Bacteria, including one cyanobacterium (and one green the “obvious” evolutionary function of a given biogeochemical alga) is not energetically coupled to photosynthesis in the sense process for the causative organisms has rarely, if ever, been di- of net autotrophic fixation of carbon dioxide (Raven 2009a.b) rectly shown to increase inclusive fitness, however obvious it (Table 1). The same applies to the bacteriochlorophyll-based may seem that the function is subject to positive selection. photochemistry in aerobic anoxygenic photosynthetic bacteria The paper emphasizes the roles of eukaryotic microorgan- that are relatively common in the surface ocean, and to some isms relative to the roles of Archaea and Bacteria in the ocean obligately anaerobic photosynthetic bacteria (Raven 2009a). and other water bodies as well as in and on rocks, soils, and In these cases the photosynthetic energy conversion functions man-made structures, making quantitative comparisons wher- in an essentially chemoorganotrophic organism to spare the use ever possible. However, it is important to acknowledge that of respiratory substrates in energizing membrane transport and there is a poorly characterized habitat, the deep subsurface bio- phosphorylating ADP. Bacteriochlorophyll-based
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