The Impact of Temperature un the Evolution of Marine Diatoms

Katrin Schmidt, Sinead Collins (University of Edinburgh, UK), Thomas Mock

Collaborating Project

Recent data on experimental evolution with eukaryotic phytoplankton have revealed that these organisms are capable of responding quickly to environmental change most likely caused by evolutionary processes other than mutations of their DNA (e.g. transposon activation, epigenetics, short non-coding RNAs). Thus, it seems that short-term acclimatory processes as part of their plastic response become accommodated very quickly and therefore significantly contribute to the evolution of these organisms. Information and insights from this project will provide first experimental evidence on how fast evolutionary processes such as epigenetics of key marine primary producers (diatoms) under global warming will impact phenotypes underpinning food web structures and biogeochemical cycles in the future ocean.

Growth Rate Temperature

Figure 1: Growth assays with evolved cell lines and the ancestral cell line (T0) of Tp (Unpublished)

There have been no studies published yet that have addressed the role of temperature for the evolution of diatoms despite the urgent need to predict the impact of global warming on the evolution and adaptation of key ecological species such as diatoms. To address this question, we have initiated a study of the evolution of two key marine diatom species to temperature. These are the temperate species Thalassiosira pseudonana (Tp) (CCMP1335) and the polar psychrophilic species Fragilariopsis cylindrus (Fc) (CCMP1102). In order to provide the material for our molecular biological and physiological investigations, we have already invested 2.5 years (e.g. 350 generations for T. pseudonana) of effort in cultivating five different biological replicates per temperature for each species. First growth assays and preliminary physiological studies were done at T0 and T350 to obtain first insights into the mechanisms of evolution (Figure 1).

Collaborating Project

This JGI (US) and NERC (UK) funded project investigates eukaryotic phytoplankton communities across latitudinal temperature zones of the Arctic and Atlantic Ocean to identify drivers of microalgae biodiversity and biogeography. Temperature is a main driving factor for species distribution on land and in the ocean. Due to global warming, ocean temperatures are rising, allowing temperate phytoplankton species expand their range further north into Polar Regions. This invasion and the sea ice retreat places polar communities at extinction risk, impacting the food web and biogeochemical cycles. We are currently lacking fundamental data on phylogenetic, functional and metabolic diversity in eukaryotic phytoplankton of the Arctic Ocean but also from temperate regions. These data are needed in order to assess and compare the current state of the different biomes and also to predict future changes in biogeochemical cycles in future changing and warmer ecosystems. This integrative project is based on metagenome and metatranscriptome sequencing of samples collected on ca. 70 stations in the Arctic and Atlantic Ocean (Figure 1). There are additional data available on important environmental variables such as nutrients, light, temperature and carbon dioxide. Currently, we are also establishing algal cultures from many of these stations.

For additional information see:

  1. School of Environmental Sciences, University of East Anglia, Norwich, UK
  2. School of Computing Sciences, University of East Anglia, Norwich, UK
  3. U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, USA
  4. University of Groningen, Netherlands
  5. Royal Netherlands Institute for Sea Research, Texel, Netherlands
  6. Alfred-Wegener-Institute, Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany
  7. The American University in Cairo, School of Science and Engineering, Cairo, Egypt
Sea of Change

Figure 1: 70 stations in the Arctic and Atlantic Ocean 

Sea of Change: Eukaryotic Phytoplankton Communities in the Arctic and Atlantic Ocean

Andrew Toseland1,2, Kara Martin1,2, Katrin Schmidt1 Kerrie Barry3, Erika Lindquist3, Susannah Tringe3, Willem H. van de Poll4, Klaas Timmermans5, Michael Ginzburg6, Ahmed Moustafa7, Klaus Valentin6, Vincent Moulton2, Igor V. Grigoriev3, Thomas Mock1

The significance of cell-wall proteins for the evolution of frustule structure and size in diatoms.

Amy R. Kirkham1, Patrick Richthammer2,†, René Hedrich2, Eike Brunner2, Karl-Heinz van Pée2, Angela Falciatore3,4, Thomas Mock1

Collaborating Project

Diatoms are unicellular algae of global ecological and economic importance. They obligately produce unique silica shells (frustules) whose intricate structures are precipitated in high order at the sub-nanometer range. This ability exceeds current capability in artificial nanotechnology. Current knowledge of the processes of diatom silica biomineralisation is based on biochemical analysis of component proteins and carbohydrates of frustules. In this project, we apply a reverse genetics approach to knock down several cell-wall proteins thought to guide structuring and precipitation of silica. This approach allows us to investigate roles for cell-wall proteins (e.g. cells size) at the organism level (Figure 1).

  1. School of Environmental Sciences, University of East Anglia, Norwich, UK
  2. Allgemeine Biochemie, TU Dresden, 01062 Dresden, Germany
  3. Université Pierre et Marie Curie, UMR7238, CNRS-UPMC, Paris, France
  4. CNRS, UMR7238, Laboratory of Computational and Quantitative Biology

† Present address: Helmholtz Zentrum Munchen, Comprehensive Molecular Analytics, Ingolstädter Landstraße 1, 85764 Neuherberg, Germany

Diatom Frustule Structure and Size

Figure 1: Phenotypic expression of cell-wall protein knock down

Whole genome expression profiling of the polar diatom Fragilariopsis cylindrus 

Jan Strauss

PhD Project Outline

A genomic analysis using RNA-Seq to investigate the adaptation of the psychrophilic diatom Fragilariopsis cylindrus to the polar environment.
Diatoms are unicellular photosynthetic eukaryotes with a silicate cell wall. They often dominate polar marine ecosystems, driving the major biogeochemical cycles in these areas. The obligate psychrophilic diatom Fragilariopsis cylindrus is a keystone species in the Southern Ocean. It thrives both in open waters and sea ice and has become a model for studying eukaryotic microalgal adaptations to polar marine conditions. The aim of this thesis was to identify how the genome of F. cylindrus has evolved to cope with marine environmental conditions of the Southern Ocean. To identify key genes, comparative genomics, high-throughput transcriptome sequencing and reverse genetics were applied. Comparative genomics with the sequenced mesophilic diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana was combined with genome-wide RNA-Seq transcriptome analysis, leading to the discovery a new bacteria-like rhodopsin not present in other sequenced diatoms. The characterisation of a bacteria-like rhodopsin in F. cylindrus was conducted by applying reverse genetics tools.

Research Project Outline

Global significance of light-driven proton pumps in eukaryotic marine phytoplankton.
Sunlight is the ultimate source of energy and a major source of environmental information for almost all living organisms. The efficient capture and use of light is a widespread and exquisitely evolved process represented across all kingdoms of life. The metabolic mode in which organisms convert light energy into chemical energy (ATP and NADPH) for growth is known as phototrophy. Two mechanistically distinct processes are known to power phototrophy. While one mechanism employs chlorophyll-containing photochemical reaction centres, the other employs rhodopsins, membrane-embedded photoreceptors composed of opsin proteins and the light-absorbing pigment retinal. Microbial rhodopsins were first discovered in purple membranes of Archaebacteria in the form of the light-driven proton pump bacteriorhodopsin and shown to generate a proton motive force across cell membranes, ultimately powering the production of ATP for energy-requiring processes in the cell. This process is independent from chlorophyll-based photosynthesis. Surprisingly, putative proton-pumping rhodopsins powering phototrophy in prokaryotes were recently also discovered in eukaryotic marine phytoplankton. However, nothing is known about their function in vivo and the role of a light-driven proton-pump in the presence of a proton gradient-generating chlorophyll-based photosynthetic apparatus remains puzzling and speculative. A better understanding of the role of rhodopsins in marine photosynthetic organisms is of global significance, because bacteria-like rhodopsins were shown to be very abundant in metatranscriptome surveys of eukaryotic marine phytoplankton and seem to be of particular significance in iron-limited areas of the ocean, accounting for 35% of the total ocean surface. Furthermore, recent studies suggest that ocean acidification due to increased dissolution of anthropogenic CO2 may decrease iron availability to phytoplankton, which may alter phytoplankton diversity in the oceans, thus, selecting for those phytoplankton species that have a competitive advantage (e.g. by the presence of bacteria-like rhodopsins) under reduced iron concentrations. Therefore we use molecular genetic approaches to elucidate the function and significance of light-driven rhodopsin proton pumps in eukaryotic marine phytoplankton.

Whole genome sequencing of the polar diatom Fragilariopsis cylindrus

Ginger Armbrust, Micaela S. Parker (University of Washington, Seattle, USA)
Chris Bowler (Ecole Normale Supérieure, Paris, France)
Klaus Valentin (Alfred-Wegener Institute for Polar and Marine Research, Bremerhaven, Germany)
Igor V Grigoriev, Alan Kuo, Erica Lindquist, Kerrie Barry (Joint Genome Institute (JGI), Walnut Creek, California, USA)

Collaborating Project

Diatoms are microscopic unicellular algae distributed throughout the world’s marine and freshwater ecosystems, including ice systems. Numerous estimates suggest that, as a group, these organisms are responsible for as much as 20% of global photosynthesis, which is comparable to the amount of primary productivity generated by all the terrestrial rainforests combined. In polar regions, where extensive permafrost and glaciers limit the amount of photosynthesis possible on land, diatoms are responsible for a huge fraction of primary productivity and therefore also for carbon sequestration. Polar diatoms are adapted to cold temperatures and high salinities and they live both within the seawater and the brine channels formed within sea ice. They serve as the base of the entire polar food web. Polar regions are displaying the greatest responses to climate change, with increased melting of sea ice and the potential disruption of this sensitive ecosystem. The whole genome sequencing of a representative polar diatom was proposed in order to gain insights into how these organisms have adapted to the extreme environments in which they thrive.

Fragilariopsis cylindrus 2 - Small

SEM of two Fragilariopsis cylindrus shells

Fragilariopsis cylindrus is regarded as a typical cold-water species found in Arctic and Antarctic sea water and sea ice. It can form large ice-edge blooms and is regularly detected in sea ice investigations. To date, prokaryotes are the only psychrophilic (cold-loving) organisms for which whole genome sequences exist. The whole genome sequencing of F. cylindrus will provide the first insights into a psychrophilic eukaryotic organism with compelling ecological and biotechnological applications. The whole genome sequences of the temperate diatoms Thalassiosira pseudonanaPhaeodactylum tricornutum, and Pseudonitzschia multiseries will provide a basis for comparative analysis with the psychrophilic F. cylindrus. The genome of F. cylindrus will provide insights into the unique physiology of polar-adapted eukaryotes and allow for better predictions of the impact climate change may have on organisms that serve as the basis for all polar ecosystems.