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Role of Chemolithoautotrophic Microorganisms Involved in Nitrogen and Sulfur Cycling in Coastal Marine Sediments

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Role of Chemolithoautotrophic Microorganisms Involved in Nitrogen and Sulfur Cycling in Coastal Marine Sediments Role of chemolithoautotrophic microorganisms involved in nitrogen and sulfur cycling in coastal marine sediments Yvonne Antonia Lipsewers THIS RESEARCH WAS FINANCIALLY SUPPORTED BY DARWIN CENTER FOR BIOGEOSCIENCES NIOZ – ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH ISBN: 978-90-6266-492-4 Cover photos: S. Rampen, L. Villanueva, M. van der Meer Printed by Ipskamp Printing, The Netherlands Role of chemolithoautotrophic microorganisms involved in nitrogen and sulfur cycling in coastal marine sediments De rol van chemolithoautotrofe micro-organismen die deelnemen in de stikstof- en zwavelcyclus in mariene kustsedimenten (met een samenvatting in het Nederlands) Proefschrift ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van de rector magnificus, prof.dr. G.J. van der Zwaan, ingevolge het besluit van het college voor promoties in het openbaar te verdedigen op dinsdag 5 december 2017 des ochtends te 10.30 uur door Yvonne Antonia Lipsewers geboren op 18 juli 1977 te Salzkotten, Duitsland Promotor: Prof. dr. ir. J.S. Sinninghe Damsté Copromotor: Dr. L. Villanueva „Hinterher ist man immer schlauer…“ Für meine Familie Table of contents Chapter 1 – Introduction .....................................................................................................1 Chapter 2 – Seasonality and depth distribution of the abundance and activity of am- monia oxidizing microorganisms in marine coastal sediments (North Sea) ..........23 Chapter 3 – Lack of 13C-label incorporation suggests low turnover rates of thaumar- chaeal intact polar tetraether lipids in sediments from the Iceland Shelf .............53 Chapter 4 – Abundance and diversity of denitrifying and anammox bacteria in season- ally hypoxic and sulfidic sediments of the saline Lake Grevelingen .......................79 Chapter 5 – Impact of seasonal hypoxia on activity and community structure of chem- olithoautotrophic bacteria in a coastal sediment .......................................................107 Chapter 6 – Potential recycling of thaumarchaeotal lipids by DPANN archaea in sea- sonally hypoxic surface marine sediments ...................................................................147 Chapter 7 – Synthesis ...........................................................................................................167 Summary ..................................................................................................................................187 Samenvatting ...........................................................................................................................191 References ...............................................................................................................................195 Acknowledgements ...............................................................................................................223 1. Introduction Marine sediments are dynamic habitats shaped by interactions of biotic and abiotic processes including the redox reactions performed by microorganisms to gain energy for growth (Schrenk et al., 2010). The biogeochemical cycling of carbon-, nitrogen- and sulfur compounds in marine sediments is tightly coupled in space and time. Due to electron donor and acceptor availability, an overlap of the activity of metabolically diverse microorganisms involved in carbon-, nitrogen- and sulfur cycling occurs. Aerobic mineralization processes of organic matter reaching the sediment surface are mainly mediated by the metabolism of phototrophic and chemoorganoheterotrophic microorganisms. These processes result in the consumption of oxygen (O2) within the first few millimeters/cen- timeters of marine sediments. Underneath the O2 penetration depth, anaerobic mineralization processes occur due to the vertical distribution of electron acceptors in the sediment: O2 → ni- − 3+ 2− trate (NO3 ) → manganese (IV) oxide (MnO2) → ferric iron (Fe ) → sulfate (SO4 ) → carbon − dioxide/bicarbonate (CO2/HCO3 ) reflecting the gradual decrease of the redox potential. Most microorganisms involved in anaerobic mineralization processes grow chemoorganoheterotro- phically, such as most denitrifying bacteria, manganese- or iron reducing bacteria, most sulfate reducing bacteria, fermenting bacteria, methane oxidizing bacteria and archaea. As a result, re- + − − duced inorganic compounds, such as ammonium (NH4 ), nitrite (NO2 ), NO3 , ferrous iron 2+ 0 (Fe ) and reduced sulfur species, such as sulfide (H2S), elemental sulfur (S ), iron sulfide (FeS), 2− 2− thiosulfate (S2O3 ) and sulfite (SO3 ), accumulate in the sediment (Jørgensen, 2006; Herbert, 1999), which can subsequently be reoxidized by chemolithoautotrophic microorganisms. Chemolithoautotrophic microorganisms (bacteria and archaea) gain energy for growth using chemical compounds as energy source (chemo-) in contrast to phototrophic organisms using light. Chemolithoautotrophs are able to use reduced inorganic compounds (litho-) as electron − donor and inorganic carbon, CO2 and/or HCO3 , as their only carbon source (-autotroph). The electron donors used by chemolithoautotrophic microorganisms comprise reduced nitrogen 2+ and sulfur compounds, as well as Fe , H2 and carbon monoxide (CO). Other microorganisms are able to assimilate organic carbon, while using inorganic electron donors, which is termed chemolithoheterotrophy, whereas those able to use inorganic or organic compounds as carbon source while utilizing inorganic electron donors are called mixotrophs. Many microorganisms use organic electron donors and fix organic carbon in a process known as chemoorganoheter- otrophy. Most chemolithoautotrophs are facultative chemolithoautotrophs, i.e. are able to grow chemolithoautotrophically as well as using a different metabolism. As chemolithoautotrophs are not able to synthesize adenosine triphosphate (ATP) from nicotinamide adenine dinucleotide (NADH) oxidation, most obligate chemolitoautotrophs couple the oxidation of their electron donors to the reduction of quinone or cytochromes supplying reducing equivalents for carbon fixation and biosynthesis through reverse electron transport (Kim and Gadd, 2008). Many per- − 2− form aerobic respiration using O2, while anaerobic chemolithoautotrophs use NO3 , SO4 , CO2 or metal oxides as electron acceptors (Jørgensen, 2006). Chemolithoautotrophic microorganisms are metabolically versatile and able to use a broad variety of electron donors for inorganic oxidation in coastal marine sediments (Table 1). Aer- obic and anaerobic ammonia oxidizing bacteria, sulfide oxidizing and sulfate reducing bacteria are believed to be the main contributors to chemolithoautotrophic carbon fixation in coastal 1 Chapter 1 2 Table 1: Versatility of chemolithoautotrophic reoxidation reactions/processes performed by microorganisms in coastal marine sediments (modified from Jørgensen, 2006). Electron donating reaction Process Chemolithoautotrophic microorganisms (e.g.) ammonia oxidizing bacteria (AOB) (Nitrosomonas), NH + + 3/ O → NO − + 2H+ +H O ammonia oxidation 4 2 2 2 2 ammonia oxidizing archaea (AOA) (Nitrosopumilus) − − NO2 + ½ O2 → NO3 nitrite oxidation nitrifying bacteria (Thiobacillus, Nitrobacter) + − NH4 + NO2 → N2 + 2H2O anaerobic ammonia oxidation anammox bacteria (Scalindua spp.) H S + 2O → SO 2− + 2H+ 2 2 4 sulfur oxidation colorless sulfur bacteria (Thiobacillus, Beggiatoa) 2− 2− 0 (other possible donors: SO3 , S2O3 , S ) denitrifying sulfur bacteria (Thiobacillus denitrificans), H S + NO − +H+ +H O → SO 2− + NH + sulfide oxidation coupled to 2 3 2 4 4 nitrate reduction to ammonia nitrate reducing sulfur bacteria (Thiomargarita), (other possible donors: S0, S O 2−) (DNRA) 2 3 large sulfur oxidizing bacteria (Beggiatoa) 4Fe2+ + O → 4Fe3+ + 2H O 2 2 iron and manganese oxidation iron bacteria (Ferrobacillus, Shewanella) (or Mn2+) 2H +O → 2H O hydrogen oxidation hydrogen oxidizing bacteria (Hydrogenobacter 2 2 2 thermophilus) 4H + SO 2– + 2H+ → 4H O + H S hydrogen oxidation coupled to some sulfate reducing bacteria (Desulfovibrio spp.) 2 4 2 2 sulfate reduction H2 + CO2 → CH4 methanogenesis methanogenic archaea 4H2 + 2CO2 → CH3COOH + 2H2O acetogenesis acetogenic bacteria Introduction marine sediments. In addition, many archaea are chemolithoautotrophs and representatives of the phylum Thaumarchaeota (formerly known as ‘marine group I Crenarchaeota’) have been determined to oxidize ammonia to gain energy for inorganic carbon fixation (Wuchter et al., 2003 and 2006; Könneke 2005, Brochier-Armanet et al., 2008) suggesting the contribution of archaea to the reoxidation of reduced inorganic compounds and inorganic carbon fixation in coastal marine sediments. Chemolithoautotrophy in coastal sediments is generally considered to be insignificant in terms of biogeochemistry, due to the low growth yields of these microorganisms and the competition with photo- and heterotrophic processes, which are the main source of labile organic matter in coastal sediments (Jørgensen and Nelson, 2004). However, although chemolithoautotrophic microorganisms might play a minor role in terms of growth, they are able to reoxidize important amounts of reduced inorganic substrates (Cypionka, 2006). The dependency of chemolitho- autotrophic microorganisms on the availability of reduced inorganic compounds produced by chemoorganoheterotrophic microorganisms suggests a tight coupling between different micro- bial metabolic pathways in marine sediments. Unfortunately, direct measurements of chemo- lithoautotrophic activity are rare. Two rate measurements
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