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Linking Microbial Communities and Macrofauna Functional Diversity With Linking microbial communities and macrofauna functional diversity with benthic ecosystem functioning in shallow coastal sediments, with an emphasis on nitrifiers and denitrifiers By Maryam Yazdani Foshtomi Promotors: Prof. Dr. Jan Vanaverbeke Prof. Dr. Magda Vincx Prof. Dr. Anne Willems Academic year 2016-2017 Thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Science: Marine Sciences Members of reading and examination committee Prof. Dr. Olivier De Clerck: Chairman Ghent University, Gent, Belgium Prof. Dr. Tom Moens: Secretary Ghent University, Gent, Belgium Prof. Dr. Nico Boon Ghent University, Gent, Belgium Dr. Melanie Sapp Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany Prof. Dr. Frederik Leliaert Botanic Garden, Meise, Belgium Ghent University, Gent, Belgium Prof. Dr. Steven Degraer Royal Belgian Institute of Natural Sciences (RBINS), Brussels, Belgium Ghent University, Gent, Belgium Prof. Dr. Sofie Derycke Royal Belgian Institute of Natural Sciences (RBINS), Brussels, Belgium Ghent University, Gent, Belgium Prof. Dr. Jan Vanaverbeke (Promotor) Royal Belgian Institute of Natural Sciences (RBINS), Brussels, Belgium Ghent University, Gent, Belgium Prof. Dr. Magda Vincx (Promotor) Ghent University, Gent, Belgium Prof. Dr. Anne Willems (Promotor) Ghent University, Gent, Belgium ACKNOWLEDGEMENTS I am deeply indebted to all my family: my lovely spouse, Mehrshad; my dearest mother and father; my siblings especially my sister, Gilda; and my in-laws for their love and support at any conditions. I would like to express my appreciation to my promotors, Prof. Magda Vincx, Prof. Jan Vanaverbeke and Prof. Anne Willems for their help and support during my PhD. It was a great honour to work under their supervision. I would like to thank all members of reading and examination committee (Prof. Olivier De Clerck, Prof. Tom Moens, Prof. Steven Degraer, Dr. Melanie Sapp, Prof. Frederik Leliaert, Prof. Sofie Derycke, Prof. Nico Boon) for their useful comments. I am very grateful to all staff of the research group Marine Biology and the Laboratory of Microbiology, Ghent University especially to Dirk Van Gansbeke and Bart Beuselinck for their technical assistance in the lab work. I would like to express my gratitude to all my Iranian friends, to my friends from Belgium, to those friends from other nationalities who I met in Belgium for their kind help. I also want to thank all my diving friends in Belgium for their warm friendship. همس کن رد نهایت ایه پایان انهم را هب پدر و مارد زعزیم، هب رم ، هب اساتیدم رد اریان و کشىرم تقدیم می م. Maryam March 2017 Table of contents Summary i Samenvatting v Chapter 1. General Introduction, Aims and Thesis Outline 1 1. Biodiversity, Ecosystem Functioning, Ecosystem Services and Ecosystem 2 Management 2. Importance of Shallow Coastal Habitats 4 3. Nitrogen Cycling Processes 5 4. Microorganisms Mediating Nitrification and Denitrification 11 5. Environmental Factors Affecting Nitrification and Denitrification 15 6. The Impact of Benthic Fauna on Nitrification and Denitrification 19 7. Aims and Objectives of the PhD Thesis 25 8. Study Area 27 8.1. Belgian Part of the North Sea (Belgium) 27 8.2. Boulogne-sur-mer (France) 28 9. Outline of the Thesis 29 Chapter 2. Variable Importance of Macrofaunal Functional Biodiversity 33 for Biogeochemical Cycling in Temperate Coastal Sediments Abstract 34 1. Introduction 35 2. Materials and Methods 37 2.1. Sampling 37 2.2. Sediment Core Incubations 38 2.3. Macrobenthos Analysis 40 2.4. Laboratory Analyses and Flux Calculation 40 2.5. Mass Budget Modeling 41 2.6. Statistical Analyses 41 3. Results 43 3.1. Spatial and Temporal Variability in Benthic–Pelagic Coupling 43 3.2. Spatial and Temporal Variability in Biogeochemical Cycling and 46 Macrobenthic Structural and Functional Biodiversity 3.2.1. Muddy Sediments 46 3.2.2. Fine Sandy Sediments 49 3.2.3. Permeable Sediments 51 3.3. Statistical Modeling of Fluxes from Abiotic and Biotic Environmental 52 Variables 4. Discussion 54 Conclusions 59 Acknowledgements 59 Chapter 3. The Link between Microbial Diversity and Nitrogen Cycling in 61 Marine Sediments is Modulated by Macrofaunal Bioturbation Abstract 62 1. Introduction 64 2. Materials and Methods 66 2.1. Study Site, Sampling and Experimental Set-up 66 2.2. DNA and RNA Extraction, PCR and RT-PCR, DGGE 69 2.3. Data Analysis 70 3. Results 71 3.1. Microbial Community Composition and Diversity Indices 71 3.2. Linking Microbial Communities with Biotic and Abiotic Sediment 76 Characteristics 3.3. Linking the N-cycle with Abiotic and Biotic Factors 78 4. Discussion 79 4.1. Effects of Abiotic Factors on Microbial Communities in the Sediment 79 4.2. Macrofauna, Microbes and the Benthic N-cycle 81 Acknowledgements 84 Chapter 4. The Effect of Bio-irrigation By the Polychaete Lanice 85 conchilega on Denitrifiers: Distribution, Diversity and Composition of nosZ Transcripts Abstract 86 1. Introduction 87 2. Materials and Methods 90 2.1. Study Site and Sampling 90 2.2. RNA Extraction and nosZ Sequencing 92 2.3. Sequence Analyses 93 2.4. Data Analysis 94 2.4.1. Environmental Data Analyses 94 2.4.2. Microbial Community Analyses and Diversity Estimates 95 2.4.3. Multiple Linear Regressions 96 3. Results 97 3.1. Sediment Environmental Factors 97 3.2. Composition of nosZ Transcripts and Diversity Indices 101 3.3. Statistical Modeling to Link Abiotic Sediment Characteristics with the 107 Diversity Indices of nosZ Transcripts in L. conchilega Reefs 4. Discussion 108 4.1. nosZ Phylogenetic Analysis 108 4.2. Horizontal and Vertical Patterns of nosZ Transcripts in Lanice 109 Aggregations 4.3. Allogenic Effect of Lanice conchilega 110 4.4. Autogenic Effect of Lanice conchilega 113 4.5. Aerobic Denitrification in Marine Sediments 113 4.6. Importance of Lanice conchilega to Denitrifiers in Relation to 114 Associated Communities in its Aggregations Acknowledgements 115 Chapter 5. General Discussion and Future Challenges 117 5.1. Biodiversity, Ecosystem Functioning, Coastal Management 119 5.2. Microorganisms and their Function 122 5.2.1. Methodological Considerations 124 5.3. The Link Between Macrofaunal Activities, Microbial Biodiversity and 130 Ecosystem Functioning in Subtidal and Intertidal Marine Sediments 5.4. Conclusions 133 5.5. Future Challenges 135 Addenda 137 Addendum 1. Appendices to Chapter 2 138 Addendum 2. Appendices to Chapter 3 148 Addendum 3. Appendices to Chapter 4 162 References 173 Publication List 232 Figures Chapter 1. General Introduction, Aims and Thesis Outline 1 Figure 1: Conceptual framework showing the links between biodiversity, 2 ecosystem functioning, ecosystem services, abiotic factors and society (modified from Duncan et al., 2015). Marine ecosystem services based on Hattan et al. (2015). Figure 2: Microbial nitrogen cycling in aquatic environments. A: nitrogen 8 + fixation; B: NOx assimilation; C: ammonification (mineralization); D: NH4 − assimilation; E: nitrification (NH3 and NO2 oxidation); F: denitrification; G: − NO3 ammonification (DNRA); H: anammox (modified after Canfield et al., 2005). Note: Ammonia is used as a substrate for the first step of nitrification (ammonia oxidation). Nitrification and denitrification processes are shown in different colours (yellow and red, respectively). Figure 3: The two steps of nitrification (ammonia and nitrite oxidation): 13 stoichiometry of reactions; genes encoding each step (amo and hao genes encoding ammonia oxidation and nxr encoding nitrite oxidation); microorganisms involved in each step (AOB and AOA: ammonia-oxidizing bacteria and archaea carry out ammonia oxidation; NOB: nitrite oxidizing bacteria involve in nitrite oxidation); and the amount of energy gained from each step (Prosser, 2005; Ward, 2008; Pester et al., 2014; Daims et al., 2015). Figure 4: The four reductive steps of denitrification (stoichiometry of 15 reactions; Zumft, 1997) and the genes (narG and/or napA, nirK or nirS, norB and nosZ) encoding the enzymes catalysing each step Figure 5: Physico-chemical factors regulating the rate of nitrification and 16 denitrification in coastal marine sediments Figure 6: Different functional groups in macrofaunal communities (Solan et 21 al., 2004; Solan and Wigham, 2005; Buatois and Mángano, 2011) and their effects (through bioturbation [particle mixing] and bio-irrigation [solute transfer]) on the physical and chemical conditions across the sediment-water interface and microbial communities in the sediment. The big arrows show solute exchange (bio-irrigation) across the sediment-water interface. Random diffusive transport of particles (bioturbation) by biodiffusers was also illustrated by white arrows. Figure 7: The biogenic mixing depth (BMD, white arrows) of sediments. A 23 and B shows BMD in two different sites. Site A is perturbed by fresh water discharge and untreated domestic sewage. Site B is identified as a pristine area. Site A harbours a lower diversity of taxa compared to the site B (Solan et al., 2004). Figure 8: Schematic overview of the macrofauna – microbiota – 26 biogeochemical processes interactions, which were studied in the present PhD thesis Figure 9: Lanice conchilega reef in the intertidal and individual polychaete 29 (modified after http://www.arkive.org/sand-mason/lanice-conchilega/ and http://borea.mnhn.fr/fr/biogenic-reefs-affect-multiple-components-intertidal- soft-bottom-benthic-assemblages-lanice-0) Chapter 2. Variable Importance of Macrofaunal Functional Biodiversity 33 for Biogeochemical Cycling in Temperate Coastal Sediments Figure 1: Bathymetry map of the Belgian Part of the North Sea with 38 indication of the sampled stations. Stations 215, ZG02 have been sampled only in June and August. 330 was sampled in June, August, and October (330). Figure 2: Chlorophyll a in overlying water (1 m above the sea floor, 45 integrated over water depth) and in the surface sediment (upper 2 cm; sqrt -2 -1 transformed for better visualization), measured SCOC (mmol O2 m d ), NHx -2 -1 effluxes, potential NOx effluxes (mmol N m d ), estimated nitrification and denitrification (mmol N m-2 d-1), and measured alkalinity flux (meq m-2 d-1) in all stations over time (mean ± SD). No data for St. 780, 120, and 130 in February.
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