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Influence of Sea Ice on Protist Community Structure in the Central Arctic Ocean

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Table of Contents Influence of sea ice on protist community structure in the Central Arctic Ocean by Kristin Hardge A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology Approved Dissertation Committee: Dr. Katja Metfies1, 2 Prof. Dr. Matthias Ullrich1 Dr. Mona Hoppenrath3 Dr. Eva-Maria Nöthig2 1 Jacobs University Bremen 2 Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Bremerhaven 3 Senckenberg Research Institute, German Centre for Marine Biodiversity Research, Wilhelmshaven Date of Defense: 10 August 2016 1 Table of Contents 2 Table of Contents “In the case of all things which have several parts and in which the totality is not, as it were, a mere heap, but the whole is something besides the parts, there is a cause.” Aristotle, Metaphysics 3 Table of Contents 4 Table of Contents Table of Contents 1 Summary ....................................................................................................................................... 7 2 General Introduction ..................................................................................................................... 9 2.1 Global warming ....................................................................................................................... 9 2.2 Changes in Arctic sea ice ........................................................................................................ 9 2.3 Protist biodiversity in the Arctic Ocean ................................................................................ 12 2.4 Protist biodiversity in the changing Arctic Ocean ................................................................. 15 2.5 Morphological and molecular methods ................................................................................. 16 2.5.1 Light microscopy ........................................................................................................... 16 2.5.2 Automated ribosomal intergenic spacer analysis (ARISA) ........................................... 17 2.5.3 Next-generation sequencing .......................................................................................... 18 3 Aims and Outline ........................................................................................................................ 21 3.1 Aims ...................................................................................................................................... 21 3.2 Outline ................................................................................................................................... 22 4 List of Manuscripts ..................................................................................................................... 24 5 Statement of Contribution ........................................................................................................... 24 6 Further Contributions .................................................................................................................. 25 7 Manuscripts ................................................................................................................................. 27 7.1 Manuscript I .......................................................................................................................... 29 7.2 Manuscript II ......................................................................................................................... 79 7.3 Manuscript III ...................................................................................................................... 125 8 Synoptic Discussion .................................................................................................................. 174 8.1 Applied methods for the assessment of protists in environmental samples ........................ 174 8.1.1 Light microscopy ......................................................................................................... 175 8.1.2 Sequencing and molecular fingerprinting ................................................................... 176 8.2 Protist communities in the changing Arctic Ocean ............................................................. 178 8.2.1 Impact of sea ice changes on protist communities ...................................................... 179 8.2.2 Influence of sea ice origin on protist communities in the sea ice ................................ 180 8.2.3 Importance of sea ice for exchange of habitat-specific protists .................................. 181 9 Outlook ...................................................................................................................................... 184 10 References ................................................................................................................................. 186 11 Acknowledgment ...................................................................................................................... 200 5 6 Summary 1 Summary The sea ice covered Arctic Ocean experiences severe and rapid changes as consequences of atmospheric and ocean warming. This is assumed to impact the protist community diversity and composition (i.e. protist community structure) in the sea ice and water column of the Central Arctic Ocean (CAO). Protists are the main food source for several trophic levels and significantly contribute to the overall productivity and functioning of the Arctic ecosystem. Thus, changes in the protist community structure would have further implications for other trophic levels and carbon sequestration. The main objective of this thesis was to elucidate the influence of sea ice change on protist community structure in several habitats of the CAO using molecular methods. In this regard, three aims were set: i) investigating the influence of different sequence processing procedures on sequencing data from protist community structure in environmental samples, ii) elucidating the impact of sea ice retreat and sea ice origin on protist communities in sea ice and water column of the CAO, and iii) analyzing the habitat-specificity of protists and their exchange between several habitats in the CAO. The fast development of Next-Generation Sequencing (NGS) involves new chances and challenges for surveillance of protists, which were addressed by the first aim of this thesis. With NGS, a large number of samples and protist communities, including small-sized (< 3 µm) and rare (< 1%) species, can be analyzed. There are several sequence processing tools and methods available to enhance sequence quality and to obtain reliable estimates of species diversity and composition (i.e. community structure). However, these procedures differ considerably from each other. The results of Manuscript I show that the protist community structure obtained with different sequence processing tools and methods is comparable for high taxonomic levels (e.g. protist phyla) and for abundant taxa (i.e. relative sequence abundance of ≥ 1%). However, a comparison with emphasis on diatom genera suggests that low taxonomic levels and particularly rare taxa (i.e. relative sequence abundance of < 1%) are highly affected by different sequence quality-checking, clustering and annotation methods. Manuscript I demonstrates that an appropriate sequence quality improvement and a phylogenetic classification of clustered sequences are the basis for a reliable estimate of the protist community structure. In addition, amplicon-based sequencing should always be accompanied by other molecular or conventional methods, such as light microscopy, to enable a critical evaluation of the results. As appropriate sequence processing tools and methods were chosen, protist communities in the changing Arctic Ocean were investigated. Within the meaning of the second aim, 7 Summary Manuscript II reports on a large-scale comparative study, which analyzed the impact of sea ice retreat and sea ice origin on protists in the sea ice and water column of the CAO. The results show that sea ice concentration and water mass origin were the main drivers for protists in the water column of the CAO in summer 2012. The sea ice community structure was significantly influenced by water mass, but more pronounced by sea ice origin. A comparison of two summer periods with contrasting sea ice concentrations (2011 and 2012) revealed that protist diversity in sea ice and water column was considerably lower during the sea ice minimum year 2012. In particular, the number of rare sea ice algae was much lower in 2012 compared to 2011, most likely due to a decrease in sea ice concentration and a reduction of diverse microhabitats. The habitat-specificity and exchange of protists in the deep-chlorophyll maximum water, under-ice water, sea ice and melt pond water were investigated in light of the third aim. The results of Manuscript III show that the sea ice was the habitat with the highest number of unique taxa. These habitat specific taxa were most likely highly-adapted to the unique environmental conditions. The results suggest that sea ice algae were released into the water column during sea ice melt. Therefore, adjacent habitats, such as under-ice water or melt ponds, play an important role in the habitat exchange. Protist occurrences and interactions between the habitats were strongly influenced by sea ice thickness and other environmental variables measured in the habitats (e.g. temperature, salinity, dissolved inorganic nutrients). The number of taxa found in all habitats (i.e.
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