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Eukaryote-Dominated Biofilms and Their Significance in Acidic Environments Sandra S

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Eukaryote-Dominated Biofilms and Their Significance in Acidic Environments Sandra S This article was downloaded by: [The University of Manchester Library] On: 17 July 2012, At: 06:56 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 Eukaryote-Dominated Biofilms and Their Significance in Acidic Environments Sandra S. Brake a & Stephen T. Hasiotis b a Department of Earth and Environmental Systems, Indiana State University, Terre Haute, Indiana, USA b Department of Geology and Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas, USA Version of record first published: 13 Sep 2010 To cite this article: Sandra S. Brake & Stephen T. Hasiotis (2010): Eukaryote-Dominated Biofilms and Their Significance in Acidic Environments, Geomicrobiology Journal, 27:6-7, 534-558 To link to this article: http://dx.doi.org/10.1080/01490451003702966 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, 27:534–558, 2010 Copyright © Taylor & Francis Group, LLC ISSN: 0149-0451 print / 1521-0529 online DOI: 10.1080/01490451003702966 Eukaryote-Dominated Biofilms and Their Significance in Acidic Environments Sandra S. Brake1 and Stephen T. Hasiotis2 1Department of Earth and Environmental Systems, Indiana State University, Terre Haute, Indiana, USA 2Department of Geology and Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas, USA Keywords algae, AMD, euglena, microorganisms, protozoan, Biodiversity of benthic eukaryotic microorganisms in highly stromatolites acidic (pH ≤ 3.5) aquatic environments is limited to species that have developed strategies to tolerate elevated concentrations of H+ and dissolved metals and low nutrients levels that commonly char- INTRODUCTION acterize these environments. To survive adverse conditions, some The purpose of this article is to provide a brief overview of algae, protozoa, and fungi have developed mechanisms to make research on the diversity of eukaryotic microorganisms in acidic their cell membranes impermeable to protons and maintain cytoso- lic pH at near neutral levels; others have developed a cell boundary systems and to discuss the potential role they may play in me- mechanism that blocks H+ ions from entering the cell. High concen- diating their environment. There is a wealth of information on trations of heavy metals are also toxic, adversely impacting growth the subject of eukaryote diversity in acidic environments, and by disrupting physiological, biochemical, or metabolic processes. this article makes no claim to be comprehensive or complete. Some algae, fungi, and protozoans are able to tolerate high metal We focus our attention, instead, on those acid-tolerant and aci- concentrations via metal complexation outside the cell, extracel- lular binding and precipitation of metals, reduced metal uptake, dophilic species commonly reported in acidic aqueous environ- increased metal efflux, and detoxification or compartmentalization ments, specifically with regard to benthic eukaryotes as opposed of metals within the cell. In acidic environments, benthic eukary- to planktonic species. We postulate, based on research to date, otic microorganisms form biofilm communities in which they are that benthic biofilm communities show the greatest potential the dominant members numerically and ecologically. Eukaryote- for mediating their environment via bioaccumulation of heavy dominated benthic communities produce heterogeneous mi- croenvironments that vary spatially and temporally in their metal and the formation of such iron-rich organosedimentary physicochemical character. The eukaryotes in these biofilms can be structures as stromatolites. considered ecosystem engineers as they directly or indirectly Highly acidic (pH ≤ 3.5) aqueous environments are common modulate the availability of resources to other species within the on Earth and originate either naturally as in volcanic springs, biofilm. These eukaryote-dominated communities may play a peat bogs, and natural acid rock drainage (ARD) or through significant role in mediating their environment by actively and pas- sively contributing to metal attenuation through various processes anthropogenic activities as in acid mine drainage (AMD) of biosorption and via formation of laminated organosedimentary and acidification of lakes and ponds (Dixit and Smol 1989; structures, which may be used as analogs for similar structures in Albertano 1995; Gross 2000; Gross and Robbins 2000). The the rock record. Downloaded by [The University of Manchester Library] at 06:56 17 July 2012 acidity of many of these environments is attributed to the pro- duction of sulfuric acid. In the case of volcanic hot springs, sulfuric acid is generated when volcanic gases of hydrogen sul- fide and sulfur dioxide react chemically and dissolve in the hydrothermal water (Iwasaki and Ozawa 1960). Received 15 September 2009; accepted 3 November 2009. In ARD and AMD environments, sulfuric acid is derived We thank G. M. Gadd and J.A. Raven for the invitation to con- tribute this review article. We thank Diane Winter for confirming our from the oxidation of sulfide minerals exposed at the Earth’s taxonomic assessment of diatoms in AMD at Green Valley. We also surface during erosion or by mining processes (Drever 1997; thank Springer for providing copyright permission to publish Figures Langmuir 1997). Surface water bodies also undergo acidifi- 1a, b, and c from Aguilera et al. (2007), and the Society for Sedimen- cation in areas where sulfur dioxide emissions from smelting tary Geology for providing copyright permission to publish Figures 4a produce acid rain (Gunn et al. 1995). These acidification pro- and d from Brake and Hasiotis (2008). Address correspondence to Sandra S. Brake, Department of Earth cesses promote ionization and dissolution of contained metals and Environmental Systems, Indiana State University, Terre Haute, in minerals that result in increased concentrations of dissolved Indiana 47809, USA. E-mail: [email protected] elements (Stumm and Morgan 1996), with iron and aluminum 534 SIGNIFICANCE OF ACIDOPHILIC EUKARYOTES 535 being highly concentrated due to their abundance in the Earth’s tary structures—that is stromatolites—in acidic environments. crust. Other such acidic water bodies as soft water lakes, which In this article we explore the potential effect of such activities are lime deficient and low in nutrients, and organic-rich bogs on acidic ecosystems. are not considered in this review article because their water chemistry is generally significantly different (e.g., Wieder 1985; Murphy 2002). SURVIVAL IN ACIDIC CONDITIONS High acidity along with elevated concentration of dissolved Such eukaryotes as algae, protozoans, and fungi are found metals is toxic to most aquatic organisms (Swift 1982). Addi- in most highly acidic environments where there is a suffi- tionally, these environments tend to be deficient in such nutrients cient energy source to sustain life, with the exception of high as inorganic carbon and phosphorus, which limits primary pro- temperature environments exceeding 60◦C (e.g., Roberts 1999; duction (Kapfer 1998; Nixdorf and Kapfer 1998). These factors Rothschild and Mancinelli 2001). For life to exist, species have also limit diversity and richness of biota to a few species of mi- developed genetic adaptations and mechanisms to tolerate the croorganisms (Mulholland et al. 1986; Verb and Vis 2000) that adverse conditions (e.g., Gadd 1993, 2007; Pick 1999; Gross include prokaryotic bacteria and Archaea (Hallberg and John- 2000). In highly acidic environments, cells must overcome the son 2003; Coupland and Johnson 2004; Druschel et al. 2004; high H+ concentration that may lead to rapid acidification of Bruneel et al. 2006) and eukaryotic algae, protozoa, and fungi the cytosol (Gross 2000), as well as develop strategies to pro- (Cooke 1966, 1976; Bennett 1969; Hargreaves et al. 1975; Al- tect themselves from adverse effects commonly associated with bertino 1995; DeNicola 2000). Most microorganisms living in acidity, such as decreased nutrients, increased dissolved metal acidic environments are acid tolerant (i.e., acidotolerant), hav- concentrations (Olaveson and Stokes 1989), and limited supply ing a wide pH tolerance with optimum growth at or near normal of CO2 for photosynthesis because of the absence of a bicar- pH, as opposed to being exclusively acidophilic with optimum bonate pool (Olaveson and Stokes 1989; Gross 2000). growth and competition under acid conditions (e.g., Gross 2000; Major
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