Source: The Conversation – France in French (2)– By Christophe Robaglia, Professor of Biology, Aix-Marseille University (AMU)
Photosynthesis fixes atmospheric carbon in the form of organic molecules essential to life and produces oxygen present in the atmosphere and in the seas. It was acquired by the living world through successive cellular integrations in “Russian doll” fashion, the photosymbioses. By mimicking the early stages of photosymbioses, we suggest, inour articlepublished inCurrent Biology, that oxygen would be a determining factor to initiate them in a hypoxic environment (that is to say, with low oxygen content) — the supply of carbon possibly being a secondary event.
By converting solar radiation into energy usable by living organisms, the photosynthesis reaction has profoundly modified the entire planet Earth. Photosynthesis allows the conversion of carbon from atmospheric carbon dioxide (CO₂) into complex organic matter, mainly in the form of sugars that feed a large portion of life forms, including human societies. Another consequence of photosynthesis, which has had major planetary-scale effects, is the production of oxygen. This is caused by the splitting of water molecules, which initiates the energy flow of electrons that enables the fixation of carbon into sugars.
Oxygenic photosynthesis appeared in a particular group of bacteria, thecyanobacteria, with fossil traces dating back 3.8 billion years and descendants still existing today. The oxygen produced allowed aerobic metabolism, more energetic, which led to the emergence of unicellular predatory organisms. Some integrated cyanobacteria, benefiting in turn from photosynthesis, this is what is calledphotosymbiosis. The distant descendants of these organisms have become the current algae and plants.
Secondary and tertiary “matryoshka” arrangements
The story doesn’t end there because, on several occasions, other predatory organisms have incorporated those already resulting from the first photosymbiosis, creating secondary and tertiary “Russian doll” nesting. For example, corals, which appeared about 500 million years ago, are animals hosting unicellular photosynthetic organisms resulting from a secondary photosymbiosis,dinoflagellates.
We have developed an experimental system allowing the laboratory evolution of early stages of the transition from a predator-prey relationship to a host-photosymbiont relationship. It includes a unicellular predator organism from the ciliate group,Tetrahymena thermophilaand photosynthetic prey. Ciliates are unicellular, very abundant in aquatic ecosystems, including paramecia. the cyanobacteriumSynechococcus elongatusallows mimicking events ofphotosymbiosisprimary and the eukaryotic green microalgaChlorella variabilisallows mimicking secondary photosymbiosis events.
Provided by the author
Thanks to the natural fluorescence of photosynthetic organisms, we combined microscopy and flow cytometry, which allows quantifying and sorting cells according to their size or fluorescence to observe the path of prey inside predator cells.
An extraordinary greed
We thus characterized this phagocytosis dynamic up to elimination in the form of fecal pellets. This showed the gluttony of the unicellular predator, which can ingest up to 160 cyanobacteria or 40 microalgae in less than an hour and gradually eliminate them over several hours. Curiously, many prey are expelled without being completely digested, or even not at all, suggesting that a simple transition between the prey state and that of an intracellular symbiont would require only the interruption of rejection.
In order to evaluate the environmental conditions allowing the initiation of symbiosis, we placed the predator and its prey in environments poor in assimilable carbon or in the absence of oxygen, and measured the survival of the predator. We thus demonstrated that photosynthetic prey considerably favor survival in hypoxic conditions, whereas they provide a weak or even nonexistent advantage in a carbon-poor environment. Hypoxia also induces a physiological condition that mitigates its own cause, since the intracellular transit of prey is considerably slowed, thereby favoring the use of oxygen produced by the photosynthesis of the prey.
This result was not really expected, as it is generally accepted that the main driver of photosymbiosis is the supply of carbon in the form of sugars. We thus show that oxygen production under hypoxic conditions can be a primary cause of the initiation of a photosynthetic symbiosis.
Hypoxic environments have been predominant for a large part of our planet’s history and are still common, particularly in aquatic and marine settings. Their incidence is even increasing under the influence of anthropogenic disturbances and rising temperatures. The exploration of these environments could therefore reveal new photosymbiotic associations. We now anticipate that the experimental system we have developed will allow us to study the molecular and cellular mechanisms stabilizing a prey as a symbiont, which remain largely unknown. Beyond understanding a fundamental mechanism of association between organisms, this work could have synthetic biology applications, for example, to build new associations producing biofuels.
Christophe Robaglia received funding from the ANR, Project-ANR-21-CE20-0035 PHOCEE
Gaël Brasseur and Loïc Quevarec do not work for, advise, hold shares in, or receive funds from any organization that could benefit from this article, and have declared no other affiliation than their academic positions.
–ref. Have oxygen-poor environments allowed the emergence of photosymbioses that changed the face of the Earth?https://theconversation.com/have-oxygen-poor-environments-allowed-the-emergence-of-photosymbioses-that-changed-the-face-of-the-earth-278135