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Diversity and Dynamics of Protist Communities in Subtidal North Sea Sediments in Relation to Metal Pollution and Algal Bloom Deposition I Annelies Pede

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Diversity and Dynamics of Protist Communities in Subtidal North Sea Sediments in Relation to Metal Pollution and Algal Bloom Deposition I Annelies Pede ! lililí UNIVERSITEIT GENT FACULTY OF SCIENCES Department Biology Research unit Protistology and Aquatic ecology Diversity and dynamics of protist communities in subtidal North Sea sediments in relation to metal pollution and algal bloom deposition I Annelies Pede Promotor: Prof. Dr. Koen Sabbe Thesis submitted in partial fulfillment of the requirements for the degree of Doctor (Ph.D.) in Science (Biology) Academic year 2011-2012 *11STQz , MIC K O M I I 4 (@ ) k FA Belgian Federal 0 . M l .Oi ’IH Science Policy V 1 Members of the examination and reading committee Prof. Dr. Dominique Adriaens (chairman) Department of Biology, Ghent University Prof. Dr. Koen Sabbe (promotor) Department of Biology, Ghent University Prof. Markus Weitere (reading committee) Helmholtz-Zentrum fur Umweltforschung (UFZ), Magdeburg, Germany Prof. Dr. David C. Gillan (reading committee) Proteomics and Microbiology Lab, Université de Mons Dr. Jan Vanaverbeke(reading committee) Department of Biology, Ghent University Prof. Dr. Wim Vyverman Department of Biology, Ghent University Dr. Julie Baré Department of Veterinary Public Health and Food Safety, Ghent University Co n t e n t s Chapter 1 1 Problem statement, aims and outline General introduction Chapter 2 15 Microbial eukaryote diversity and community structure in relation to natural stressors and trace metal pollutants in subtidal coastal marine sediments (North Sea, Belgium). Chapter 3 51 Effects of spring phytoplankton bloom deposition on seasonal dynamics and vertical distribution of microbial eukaryotes in a silty, metal-contaminated sediment in the southern North Sea. Chapter 4 79 Effect of bacterial mineralisation of phytoplankton-derived phytodetritus on the release of arsenic, cobalt and manganese from muddy sediments in the Southern North Sea. A microcosm study. Chapter 5 103 Impact of phytoplankton bloom deposition and concomitant metal fluxes on the composition and activity of benthic microbial communities in subtidal marine sediments: a microcosm study. Chapter 6 133 Short-term response of active microeukaryotic communities to arsenic (KH2ASO4) contamination in silty and sandy subtidal coastal marine sediments. Chapter 7 159 General Discussion Future Perspectives Summary 271 Samenvatting 275 References 179 Problem statement, aims and outline The pollution of marine ecosystems by trace metals is a world-wide problem (Boran & Altinok, 2010). Trace metals (TM) are toxic for many life forms, including humans (a.o. via fisheries). In coastal environments, TM are mainly bound in silty, organically enriched sediments, and changes in the environment can lead to the resuspension of the metals (Eggleton & Thomas, 2004), with the activity of the benthic microbes as one potential factor influencing the release of TM into the water column (Eggleton & Thomas, 2004). Benthic microbial activity and dynamics in turn are regulated by the availability of growth substrates, and sedimentation of algal blooms represents a major source of organic material for the benthic biota in subtidal areas (Boon, et al.,1999). It remains unclear however, how microbial communities, phytodetritus deposition and TM behaviour interact in subtidal sediments. The overall objective of this thesis is to obtain a better insight in the interactions between microbial communities, metal contaminants and algae-derived organic matter in contaminated marine sediments in the Belgian Coastal Zone (BCZ). The thesis was carried out in the framework of the MICROMET project (Microbial diversity and Metal fluxes in contaminated North Sea sediments), supported by funding from the Belgian Federal Science Policy Office (SD/NS/04A & 04B), in the frame of the SDD programme (the ‘Biodiversity’ & ‘Marine Ecosystem’ domains). While our project partners focused on prokaryotic communities and sediment biogeochemistry, we focused on the dynamics, role and response of benthic protist communities in the above-mentioned interactions. Protists are eukaryotic unicellular organisms who occupy a central position in benthic food webs, and especially in the microbial loop. We first described the spatial and temporal variation of these communities in relation to the abiotic and biotic subtidal benthic environment (including TM). We then documented how the microbial communities (both pro- and eukaryotic) respond to algal bloom deposition, and how this affects TM mobilization. Finally, we tested the direct effect of high concentrations of the toxic TM arsenic (As) on the protist communities. This research was performed in two phases: The first phase of this thesis was based on field observations. We studied the diversity and spatio-temporal variation in benthic protist communities in the BCZ using 18S rDNA-based molecular fingerprinting techniques (DGGE) and clone libraries, and then identified the factors potentially regulating their dynamics using multivariate statistics. In Chapter 2, microeukaryotic community composition was compared between the oxygenated top layer and anoxic bottom layer of sediments from 9 BCZ stations with different granulometries and TM loads, before and after the spring phytoplankton bloom in 2007. In Chapter 3, we present a more detailed, monthly analysis of protist community variation with depth ( 0-10 cm) in one silty, metal-contaminated station, for the period February to July 2008. The second part of this thesis deals with two separate microcosm experiments in which sediment cores were incubated under various environmental conditions, viz. with and without phytodetritus deposition, and at a range of As concentrations. This not only allowed giving a more detailed picture about the direct response of benthic microbial communities to organic matter enrichment and metal contamination, but also to assess the potential role of microbial communities to metal mobilization. We studied both total and active communities based on SSU rDNA and SSU rRNA respectively. In Chapter 4 and Chapter 5, we performed a microcosm experiment in which the deposition of a phytoplankton bloom was simulated in metal-contaminated sediment cores. Total and active prokaryotic and microeukaryotic communities were studied simultaneously during 7 days, and related to TM dynamics during increased phytodetritus mineralization. The response of microbial activity and community composition are discussed with respect to the microbial loop, the enrichment effect and the metal fluxes. Chapter 6 focuses on the acute effect of As intoxication after two days of incubation of sediments contaminated with a series of arsenic levels (control, 60, 120, 240, 480 and 960pg If1). The response of the active protist community was evaluated and compared between two stations with a different granulometry and contamination history: one station with silty sediments and high background As concentrations, and the other station with sandy sediments and low background As concentration. The main conclusions are summarized and discussed in Chapter 7, and perspectives for future research are provided. All the chapters excluding the introduction (chapter 1), discussion (chapter 7) and summary are manuscripts in preparation. The first author analysed the protist samples and data and wrote the chapters, except when stated otherwise. 1 General Introduction In this introduction, I first give a description of coastal subtidal marine sediments (biogeochemistry and biota, with special attention to benthic protist communities), then I give an introduction to trace metal (TM) toxicity and factors affecting the release and bioavailability in marine sediments (with emphasis on microbial activity), and finally the study area, i.e. the Belgian Coastal Zone (BCZ) is described in terms of the sediment environment, phytoplankton blooms and TM pollution. Marine subtidal sediments Marine subtidal sediments are important as a permanent or temporary (e.g. resting stages; McQuoid, 2002) habitat for many benthic and planktonic organisms. Biogeochemical processes in marine sediments are strongly linked to processes and conditions in the water column (Middelburg & Levin, 2009). Marine coastal areas are often highly productive, which causes high fluxes of organic matter (OM) to the sediment (Boon, 1998). Intense mineralization of this OM takes place in the sediments; as a result, a large part of the coastal carbon and nutrient cycles can take place in the benthic ecosystems (Patterson, 1989, Ehrenhauss, et al. ,2004, Lancelot et al. ,2005), making marine subtidal sediments crucial for global biogeochemical cycling (Orcutt, et al.,2011). Sediment types (sandy vs. silty) Many coastal areas are characterised by sediments with different grain size composition, mainly resulting from local hydrodynamic conditions. Fine sediments are mainly found in more sheltered sites, since small particles are readily maintained in suspension by turbulence (Fenchel, 1969). The size of the particles influences the porosity, permeability, and capillarity of the sediment. These factors (especially permeability) are important because they determine the behaviour of the interstitial water and thus the availability of oxygen (Fenchel, 1969). Bottom-water oxygen availability is one the main factors governing diagenetic pathways, sediment biogeochemistry and mineralization rates, and sediment-water exchange fluxes, as 1 Chapter 1 well as the biotic communities that influence these processes (Ehrenhauss, 2004, Fenchel & Finlay, 2008, Glud, 2008). Sandy sediments are permeable and permit porewater flows that transport oxygen, as well as dissolved and
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