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Carbon Cycling and Calcification in Hypersaline Microbial Mats

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Carbon Cycling and Calcification in Hypersaline Microbial Mats Carbon cycling and calcification in hypersaline microbial mats Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften - Dr. rer. nat.- Dem Fachbereich Biologie/Chemie der Universität Bremen vorgelegt von Rebecca Ludwig Bremen März 2004 Die vorliegende Arbeit wurde in der Zeit von Oktober 2000 bis März 2004 am Max-Planck-Institut für marine Mikrobiologie in Bremen angefertigt. Gutachter Prof. Dr. Bo Barker Jørgensen Prof. Dr. Gunter O. Kirst Prüfer Prof. Dr. Friederike Koenig Dr. Henk M. Jonkers Tag des Promotionskolloqiums: 14. Mai 2004 Table of contents Table of contents Thesis outline v 1 Introduction 1 Prologue 3 Carbon cycle in microbial mats: Organisms and metabolism 8 Gradients and adaptations to diel changes 17 Calcification 20 Principles and applications of microsensors 22 Sampling/study sites 28 2 Structure and function of Chiprana mats 37 Structural and functional analysis of a microbial mat ecosystem from a unique permanent hypersaline inland lake: ‘La Salada de Chiprana’ (NE Spain) 3 Rate limitation in microbial mats 71 Limitation of oxygenic photosynthesis and respiration by phosphate and organic nitrogen in a hypersaline mat: A microsensor study 4 Effect of salinity on benthic photosynthesis 89 Reduced gas diffusivity and solubility limit metabolic rates in benthic phototrophs at high salinities 5 Calcification mechanism in a microbial mat 109 Photosynthesis controlled calcification in a hypersaline microbial mat 6 Stromatolite calcification and bioerosion 127 Balance between microbial calcification and metazoan bioerosion in modern stromatolitic oncolites Discussion 145 Summary 151 Zusammenfassung 153 Appendix 155 Danksagung 155 List of publications 157 iii Outline Thesis outline Five manuscripts are included in this thesis that investigate the carbon cycle in microbial mats with a special emphasis on community carbon flow and mechanisms of microbial calcification. The introduction (chapter 1) provides background information about organisms and processes involved in the carbon cycle in microbial mats. Emphasis was placed on oxygenic photosynthesis, the dominant primary production process in mats, and its relation to the organic carbon cycle. Chapter 2 describes the microbial mats from “La Salada de Chiprana” with special emphasis on the structural and functional analysis of the microbial community with respect to the carbon cycle. Concept developed by Rebecca Ludwig and H. Jonkers, execution and data analysis by Rebecca Ludwig and H. Jonkers with help of the respective co-authors. The manuscript was written by H. Jonkers with editorial help from Rebecca Ludwig. Published in FEMS Microbial Ecology. Objective of the study presented in chapter 3 was the identification of factors that limit oxygenic photosynthesis and respiration in microbial mats of “La Salada de Chiprana”. The study was initiated by H. Jonkers and O. Pringault. Rebecca Ludwig was responsible for the execution, data analysis and interpretation. The manuscript was written by Rebecca Ludwig with editorial help from H. Jonkers. The manuscript has been prepared for submission to FEMS Microbial Ecology. Chapter 4 compares the influence of salinity on photosynthesis and respiration between planktonic and benthic model cultures of Cyanothece sp. (PCC 7418). The concept was developed by F. Garcia-Pichel and Rebecca Ludwig. The experiments were executed by Rebecca Ludwig. The manuscript was written by Rebecca Ludwig with editorial help from F. Garcia-Pichel. The manuscript is in preparation for submission to L&O. v Outline The study described in chapter 5 investigated whether calcification in mats from “La Salada de Chiprana” is driven by photosynthetic or heterotrophic processes. Rebecca Ludwig and H. Jonkers developed the concept. Execution, data analysis and interpretation by Rebecca Ludwig. The manuscript was written by Rebecca Ludwig with inputs from the co-authors. This manuscript is to be submitted to L&O. Chapter 6 examines the balance between calcification and metazoan grazing in stromatolitic microbialites from Cuatro Cienegas, Mexico. The study was initiated by F. Garcia-Pichel. Rebecca Ludwig and F. Al Horani were responsible for concept, execution and data analysis of microsensor measurements. All authors contributed equally to this work. Published in Geobiology (in press). vi Chapter 1 Introduction 1 Introduction Prologue: Ancient and modern microbial mats Microbial mats are dense aggregations of microorganisms and their viscous excretion products that form a laminated system at the boundary between a substratum (typically the sediment surface) and water1. The lamination of phototrophic microbial mats originates in the vertical distribution of pigmented bacteria, which orient themselves to zones where they find optimal conditions. Mats harbour a large diversity of microbes, which by their metabolic activity create steep chemical gradients2. Microbial mats are considered to be analogues of ancient stromatolites (Fig. 1) and have been extensively researched in order to better understand the formation of the latter (Van Gemerden 1993). While similar to microbial mats, stromatolites are solid structures as a consequence of heavy calcification or sediment trapping. Stromatolites represent the first fossilised evidence for life on earth, and have been found in rocks as old as 3.2 Ga (1 Ga = 109 years) (Nisbet & Fowler 1999). Stromatolites claimed to be older than that might be structural analogues of abiotic origin (Lowe 1994). Geological evidence suggests that life originated even earlier, around 3.8 – 4 Ga, without leaving a fossilised trace (Nisbet & Sleep 2001; Nisbet & Fowler 2003). Where exactly life originated, what kind of metabolism was used and what early life looked like are topics heavily disputed and controversially discussed. Due to scarce evidence these questions might never be answered unambiguously and scientists are left to develop scenarios for the evolution of life based on indirect evidence about early earth (i.e. ancient relics, modern descendants, models) (Nisbet & Fowler 2003). The best way to avoid misinterpretation of the scarce evidence might be the integration of evidence from geology, biochemistry and (molecular) biology. As recent microbial mats are often considered as analogues of ancient stromatolites this prologue presents some aspects of the environmental conditions ancient stromatolites probably experienced and the metabolic processes that might have taken place. Soon after the origin of earth around 4.6 Ga the earth was very hot and reached core temperatures of around 2000°C, the melting temperature of iron. Due to gravitation, 1 While this is also true for biofilms, most researchers reserve the term mat for a system with a visible lamination. 2 For a more detailed description of organism and processes in microbial mats the reader is referred to the following section. 3 Chapter 1 the heavy liquid iron accumulated in the core, while lighter material got transported towards the surface where it cooled down and built a thin crust. To our present knowledge, the existence of liquid water and an atmosphere is essential for the existence of life. Both the gaseous atmosphere and liquid water are thought to have gassed out from the hot core of earth, where they were present in elemental form (Press & Siever 1995). The exact nature of this prebiological atmosphere is heavily debated, but the favoured hypothesis today is that it was mildly reducing with N2 as the major constituent but also containing CO2 and H2O (Wayne 2000). It had been assumed previously that the prebiological atmosphere mainly contained NH3 and CH4 and was strongly reducing, but recent research suggests that these constituents did not last long, if they were present at all (Wayne 2000; Nisbet & Sleep 2001). This is supported by highly metamorphosed sediments in Isua, West Greenland (3.8 Ga), that are thought to be formed in the presence of H2O and CO2, but without abundant methane (Wayne 2000). As mentioned above, life probably originated around 3.8 – 4 Ga, but whether this happened in hydrothermal or mesophilic environments is heavily debated3. While this question cannot be fully answered based on the evidence known so far, one possible scenario for the evolution of life, namely the evolution of mats around hydrothermal vents, will be described4. Hydrothermal vents would have allowed chemolithoautotrophs to thrive as they transport reduced compounds like H2, H2S, CH4 from the earth’s core to the more oxidised ocean waters (Nisbet & Fowler 2003). The earliest organisms might have been using FeS and H2S to gain energy or H2 and CO2 for methanogenesis. As death should have been part of life from its start, the biomass of these bacteria would for example enable fermenters to live on dead organic material. This might indeed have been an important source of organic carbon, as the existence of a primaeval soup of organic carbon is challenged by geologists (Martin & Russell 2003; Nisbet & Fowler 2003). Some sulphate and nitrate was probably provided via the atmosphere (Nisbet & Fowler 2003) and allowed anaerobic respiration e.g. by sulphate reducers which might have had evolved around 3.5 Ga ago (Shen et al. 2001). Anaerobic respiration in turn would have provided reduced 3 One argument used to support a hyperthermophilic origin is that the most deeply rooted organisms of the universal phylogenetic tree are high temperature adapted (Pace 1997; Woese 2000; Nisbet & Fowler 2003), however, the inferred GC content of the universal ancestor and
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