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The Matryoshka principle of green symbiosis

Unicellular, aquatic dinoflagellates are masters of what is known as nested symbiosis. They engulf chloroplast-carrying organisms which enable them to photosynthesize sunlight. While this type of symbiotic relationship enables dinoflagellates to survive, the toxins produced by algal blooms, which typically involve dinoflagellates, can have a deadly effect on marine life. This in turn can also affect organisms that consume marine life – including humans. Researchers at the University of Stuttgart are studying the variety and complexity of such symbiotic life forms.

Dinoflagellates and ciliates live in nested symbiosis. The photo shows Mesodinium rubrum, which is a major cause of red tides. The ciliate contains a eukaryotic endosymbiont which itself also contains a eukaryotic endosymbiont. The latter contains a chloroplast derived from a bacterial endosymbiont. Blue = nuclei, green = chloroplast, yellow= mitochondria. The seven DNA-containing cell compartments are shown in red. © Schweikert, University of Stuttgart

Blooms of harmful algae (BHA) can have a huge impact on aquatic ecosystems, and hence on all types of aquafarming, including shellfish and fish farming. BHA can be associated with high commercial losses when aquafarms are unable to supply the increasing quantities of fish and seafood required for human consumption. In extreme cases they have fatal consequences for both fish and shellfish - as well as human consumers. Algal blooms tend to occur close to the coast where many shellfish and fish farms are located. The blooms do not impact on traditional fishing as wild fish can easily avoid locally restricted algal blooms. Harmful algal blooms are the result of the rapid increase and accumulation of dinoflagellates, single-celled eukaryotes which are major components of phytoplankton. 

“Algal blooms are caused by dinoflagellate species that reproduce in large numbers under favourable nutrient, light and temperature conditions. Such algal blooms tend to occur for example twice a year in the North Sea, in spring and autumn. In addition, the pollution of water with fertilizers (phosphates, nitrates) also encourages algal blooms. For example, the inflow of untreated wastewater into estuaries provides high levels of nutrients, which favours the mass reproduction of dinoflagellates,” said PD Dr. Michael Schweikert from the Institute of Biology at the University of Stuttgart, explaining the mechanisms of algal blooms. Schweikert’s research is focused on the taxonomy of dinoflagellates and their symbiotic relationships with other organisms. This work, which is part of a project funded by the BMBF (German Federal Ministry of Education and Research), has, along with other findings, provided scientific evidence of the close connection between agricultural wastewater inflow and algal blooms that occur in Scottish coastal waters. To counteract the situation, many aquafarms have been moved from the North Sea to the Atlantic despite the rough waters that create less favourable aquafarming conditions.

Symbiosis is key in the occurrence of algal blooms

The dashed lines highlight endosymbioses known to occur in ciliates and dinoflagellates. Dinoflagellates can also live as endosymbionts in other animals like corals for example. © Schweikert, University of Stuttgart
“With respect to algal blooms, the term “algal” is not used in a taxonomic sense, instead it denotes a kind of “profession” that is common to all photosynthetically-active species that are part of algal blooms. Around 80 percent of all harmful algal blooms are caused by dinoflagellates whose chloroplasts enable them to carry out photosynthesis from which they obtain the energy needed for survival,” said Schweikert explaining why he believes that the term “algal bloom” is misleading. “Around half of all living species of dinoflagellate possess chloroplasts that originate from symbioses with other organisms; the other half are non-photosynthesizing heterotrophs that have most likely lost their previously acquired chloroplasts,” Schweikert explains. Unicellular eukaryotes constitute their own phylogenetic group that has given rise to the plant and animal kingdoms. “Heterotrophic dinoflagellates were traditionally classified as “animal-like” protozoans and dealt with by scientists working in the field of protozoology while research on the “plant-like” chloroplast-carrying dinoflagellates was part of phycology, a subdiscipline of botany. Dinoflagellates were thus either classified as Dinophyta or Dinoflagellata. Nowadays the term “protozoan” is rarely used to classify dinoflagellates; instead, it is now widely accepted that all single-celled organisms other than bacteria, including the division of Dinoflagellata, are part of the Protista kingdom. Protists are organisms that do not fit into the animal or plant kingdoms,” explains Schweikert. Many scientists working with dinoflagellates have a knowledge of botany and zoology that facilitates their work on dinoflagellates, which can switch between “plant-like” and “animal-like” due to their ability to lose and incorporate chloroplasts. Modern dinoflagellate classification is also based on the finding that dinoflagellates have a common phylogenetic origin, i.e. belong to the same group of organisms for morphological, physiological and molecular reasons.

An old model: from symbiosis to organelle

Endosymbioses between dinoflagellates and other organisms have many variations. For example, dinoflagellates can incorporate and form symbiotic relationships with phototrophic bacteria and single-celled eukaryotic organisms. These organisms are taken up by way of phagocytosis, a process by which the cell membrane engulfs solid particles/cells and causes an internal phagosome to form. Phagocytosis is a size-selective process, which means that dinoflagellates can engulf any single-celled species as long as it is the appropriate size. Biochemical signalling pathways also appear to exist between dinoflagellates and the engulfed organisms that prevent the latter from being digested. The engulfment leads to a permanent endosymbiotic relationship that is mutually beneficial to both organisms: the dinoflagellates use the photosynthetic products of the microsymbionts and the microsymbionts benefit from the CO2 arising from the respiratory chain of the dinoflagellates. Future research will provide further insights into the diversity of the mutual relationships that exist between dinoflagellates and microsymbionts.

One such example is the symbiotic relationship between cyanobacteria and dinoflagellates that result in the bacteria’s loss of independence as the dinoflagellate cells continue to undergo millions of cell division rounds. “The engulfed bacterium becomes more and more dependent on its host and evolves into a cell organelle, in this case a chloroplast, which encodes only a few of the genes required for proper chloroplast function,” said Schweikert. Chloroplast-carrying dinoflagellates are able to carry out photosynthesis; most of these are mixotrophic, combining photosynthesis with the ingestion of prey. The issue becomes truly exciting in the case of the dinoflagellates that take up chloroplast-carrying eukaryotes (e.g. diatoms) but do not digest them. “The engulfed eukaryotes continue to take up other organisms such as cyanobacteria. This process can continue and eventually lead to secondary, tertiary and even quarternary endosymbioses, which makes it increasingly difficult for us to identify the organism from which the chloroplast originates. The only way for us to find out whether the chloroplast originates from primary, secondary, tertiary or quarternary endosymbiosis is to count the cell membranes of the chloroplast,” Schweikert explains.

A cell engulfs a cell, which is then engulfed by another, and so on….

These endosymbiotic processes lead to a broad range of genetic combinations. “The chloroplast possesses its own bacterial DNA, the dinoflagellate possesses nuclear and mitochondrial DNA, as does the second eukaryote that was engulfed by the dinoflagellate. Over time, the symbiotic organisms exchange genetic material with each other in a process known as lateral gene transfer. A large amount of the original genes present in the engulfed endosymbiont disappears. We have found dinoflagellates in all kinds of intermediary stages,” Schweikert explained. Dinoflagellates make intensive use of the photosynthetic system that they acquired along with the engulfed cyanobacteria and other photosynthetic organisms. The process of gaining photosynthetic abilities through the engulfment of photosynthetic organisms is a rapid evolutionary event rather than a linear one. The entire system is subsequently subject to evolutionary selection, which sometimes gives rise to dinoflagellates with the advantageous property of being able to thrive and accumulate under favourable environmental conditions and form harmful algal blooms.

Due to the complexity of these systems, even state-of-the-art methods are unsuitable for directly counteracting the development of algal blooms, particularly as the underlying mechanisms are not yet known in detail. Schweikert explains that this does not make sense from a practical point of view either: “Interfering with the biology of the dinoflagellate population is rather expensive. In addition, the ocean is so vast that such an intervention becomes impossible. But we can monitor the situation and issue early warnings about algal blooms. This already works quite well, but researchers around the world still need to work on the fine tuning of such monitoring procedures,” Schweikert said. Amongst other things, further taxonomic studies, in which Schweikert is also involved, are needed.

Research into dinoflagellate symbioses has major potential, in particular as far as biotechnological and systems biology investigations are concerned. Endosymbiosis leads to the creation of a new compartment in single-celled eukaryotes, a process that can be used as a model for research into the use of eukaryotic unicellular organisms in bioproduction. “Although eukaryotes are more difficult to grow than bacterial cultures, they are nevertheless used in situations where prokaryotes cannot be used,” Schweikert explained.

Further information:
University of Stuttgart
Institute of Biology, Department of Zoology
PD Dr. Michael Schweikert
Pfaffenwaldring 57
70569 Stuttgart
Tel.: +49 (0)711/ 6856 5085
E-mail: Michael.Schweikert(at)bio.uni-stuttgart.de

Website address: https://www.biooekonomie-bw.de/en/articles/news/the-matryoshka-principle-of-green-symbiosis