Biodiversity, phylogeny, biogeography and ecophysiology of benthic diatoms from the West Antarctic Peninsula

Abstract

Polar regions play a critical role in the Earth’s climate system and global nutrient circulation and comprise many different habitats with unique organisms. The seasonal change from the polar night to the midnight sun distinguishes the polar regions from all others of the world. The marine organisms living in these regions have to cope with extreme seasonality of light, temperature, salinity and sea ice. One ecologically particularly important group of eukaryotic microorganisms in polar shallow water coastal zones are benthic diatoms. Diatoms are among the largest and ecologically most successful groups of protists, as they are widespread in almost all aquatic habitats on Earth and contribute significantly to annual carbon fixation. Despite their influential ecological role, there is still little information on their biodiversity in the polar seas. The Diatom Research group of the Botanic Garden and Botanical Museum Berlin in cooperation with the Applied Ecology and Phycology group of the University of Rostock initiated a first study to expand the knowledge about the biodiversity of benthic diatoms in Antarctica by using a combined approach of morphology, culturing and DNA metabarcoding. This project was funded by the Priority Program “Antarctic Research with Comparative Studies in Arctic Ice Regions” of the German Research Foundation. Benthic samples from marine, brackish and freshwater habitats were collected in Potter Cove, King George Island on the Antarctic Peninsula. 162 clonal cultures were successfully established at the Botanic Garden Berlin, resulting in the identification of 60 taxa. A taxonomically validated reference library for Antarctic benthic diatoms with comprehensive information on habitat, morphology and DNA barcodes (rbcL and 18SV4) was created. Three of the most abundant species were Navicula cf. perminuta, Nitzschia annewillemsiana and Navicula gregaria in marine, freshwater and brackish water habitats, respectively. Combining the total morphological richness of 174 taxa, including clones, with an additional 72 taxa assigned by metabarcoding only, resulted in 238 taxa in total. Taxa, which could be assigned on species level showed a high level of endemicity. Finally, all reference sequences were linked to diatom specimens deposited in the Herbarium Berolinense to ensure a complete chain of evidence and further subsequent investigations. The barcode reference library of Antarctic species made it possible to assign 47 taxa in the metabarcoding analyses that could not be assigned previously because no suitable reference sequences were available. Two taxa, Planothidium wetzelii and Chamaepinnularia australis, were newly described within this thesis. The separation of both taxa was only possible by the combined investigation of morphological and molecular traits, which highlights the importance of an integrative taxonomy for diatoms. Chamaepinnularia australis belongs to a genus that is frequently found in the Antarctic and Arctic. Since its first description almost 30 years ago, its position in the diatom tree of life remained uncertain. Molecular phylogeny in combination with the study of morphological features revealed the monophyly of this genus and its allocation to the Sellaphoraceae family. Molecular data are valuable for determining the phylogenetic position of diatom taxa and have proven particularly useful for genera that have been difficult to classify solely based on morphological characters. The clonal diatom cultures have been integrated into the culture collection of the University of Rostock and have been successfully used for ecophysiological studies. The exposure of five strains to total darkness over a period of three months showed that the utilization of storage lipids is one of the key mechanisms in Antarctic benthic diatoms to survive the polar night. Despite an ultrastructural observable degradation of the chloroplast, photosynthetic performance did not change significantly. Further, photosynthesis, respiration, and growth response patterns were investigated as functions of varying light availability, temperature, and salinity in six benthic diatom strains. All of them showed a high ecophysiological plasticity with activity patterns exceeding the environmental range they usually experience in situ. This may represent an important trait to cope with climate change in the Antarctic Peninsula. A thorough taxonomic investigation combined with the evaluation of the biogeographical expansion of a species is required as a baseline for ecophysiological experiments to draw sound conclusions about their adaptation to environmental conditions. To summarise, this project has revealed a remarkably high benthic diatom diversity in the coastal areas of Antarctica. Still, many species are not yet recorded in reference databases. Furthermore, the metabarcoding results indicate a high cryptic diversity with many unassigned taxa even on genus level, which emphasises the need for a further intensive taxonomic investigation of benthic diatom in this region. The genotypic data obtained by DNA barcoding combined with phenotypic information obtained by studying the morphology of marine benthic diatoms are urgently needed to improve our fundamental understanding of the biodiversity and biogeography of diatom communities in the Antarctic. Such data sets not only provide a basis for biodiversity studies, but also for future monitoring programmes, e.g. when investigating the effects of coastal erosion on the benthic diatom flora, for geological questions on the reconstruction of the palaeoenvironment and for the effects of climate change.