1. Biochemistry and Chemical Biology
  2. Plant Biology
Download icon

Photosynthesis: Oxygen overload

  1. Britta Foerster  Is a corresponding author
  1. Research School of Biology, Australian National University, Australia
Insight
  • Cited 0
  • Views 522
  • Annotations
Cite this article as: eLife 2021;10:e75695 doi: 10.7554/eLife.75695

Abstract

A structure that helps algae photosynthesize when carbon dioxide levels are low may also play a role during hyperoxia conditions.

Main text

Bioreactors of algae are commonly used to generate biomass, a renewable source of energy. To do this, scientists exploit the algae’s ability to efficiently convert carbon dioxide into organic compounds, such as sugar, using photosynthesis. This process is known as carbon fixation and requires high levels of inorganic carbon in order to be successful. If the primary enzyme involved in this reaction – called Rubisco (short for ribulose-1,5-bisphosphate carboxylase/oxygenase) – does not receive enough carbon dioxide, it mistakenly fixes oxygen instead. This results in unfavourable by-products that inhibit photosynthesis and require lots of energy to recycle (Peterhansel et al., 2010).

To overcome this problem, algae evolved a carbon dioxide concentrating mechanism (CCM) that allows the rate of photosynthesis to remain high despite low levels of inorganic carbon (Badger and Price, 1992; Raven et al., 2017). Much of what is known about the CCM has come from studying a single cell alga known as Chlamydomonas (Mackinder et al., 2017). These studies revealed two key components that allow the CCM to increase the concentration of carbon dioxide around Rubisco enzymes: transporter proteins that pump carbon dioxide into the chloroplast, and structures called pyrenoids which sequester Rubisco enzymes. Pyrenoids are condensed proteins which are often surrounded by a starch sheath that promotes the selective entry of carbon dioxide and shields Rubisco from oxygen. However, the mechanisms and signals underlying the formation of these pyrenoids have largely remained elusive.

Past and current research has mostly focused on pyrenoids that appear when CCMs are induced by low levels of inorganic carbon (Wang et al., 2015). Now, in eLife, David M Kramer (Michigan State University) and colleagues – including Peter Neofotis (also from Michigan State) as first author – report that pyrenoids may also be induced by high levels of oxygen, in the absence of other CCM components (Neofotis et al., 2021).

The team – which included researchers from Michigan State and ExxonMobil – found that a species of alga called Chlamydomonas reinhardtii contains pyrenoids when there are extremely high levels of oxygen in the air (also known as hyperoxia) despite carbon dioxide levels also being high (Figure 1). The structure of these oxygen-induced pyrenoids is strikingly similar to those formed in response to low levels of inorganic carbon. This led Neofotis et al. to hypothesize that the signal that induces pyrenoid formation may be produced when photosynthesis takes place either under hyperoxia conditions or when there are low levels of carbon dioxide.

How hydrogen peroxide stimulates the formation of pyrenoids under different conditions.

Depicted are typical Chlamydomonas cells with a single cup-shaped chloroplast (green) and a nucleus (grey circle, N). When carbon dioxide (CO2) levels in the air surrounding the alga are higher than oxygen (O2; top), Rubisco enzymes (blue and yellow) are dispersed in the chloroplast and efficiently fix carbon dioxide. When carbon dioxide levels are lower than oxygen (left), Rubisco fixes oxygen instead. This leads to harmful metabolites that need to be recycled, resulting in the generation of the by-product hydrogen peroxide (H2O2; orange). To counteract this, Chlamydomonas employ a carbon dioxide concentrating mechanism (CCM) which sequesters Rubisco enzymes in to pyrenoids that preclude the entry of oxygen (grey circular structure), and produces proteins that transport carbon dioxide into the chloroplast (Ci; purple). When oxygen levels are high (also known as hyperoxia; right), this leads to oxygen fixation and production of hydrogen peroxide as well. Neofotis et al. found that Chlamydomonas also contain pyrenoids under these conditions, even when there are high amounts of carbon dioxide and the full CCM is suppressed. This led them to propose that hydrogen peroxide triggers the formation of pyrenoids via an unknown mechanism when oxygen levels are high and when there are insufficient amounts of carbon dioxide.

Image credit: Britta Foerster (CC BY 4.0)

The signalling molecule hydrogen peroxide was considered to be the strongest candidate for the role as it is a by-product of oxygen fixation, a scenario that can occur when oxygen levels are high or when there are insufficient amounts of carbon dioxide (Figure 1). Further experiments showed that hydrogen peroxide levels and the formation of pyrenoids are highly correlated, providing strong evidence for this hypothesis.

To address the role pyrenoids play under high oxygen stress, Neofotis et al. studied and compared Chlamydomonas strains which have varying tolerance to hyperoxia. The experiments showed that the pyrenoids found in these genetic variants have different structures and sometimes fail to form a sheath. Algae that could endure high levels of oxygen and formed fully starch-sheathed pyrenoids had significant growth advantages over those that had more fragmented and poorly developed sheaths. This is consistent with the theory that pyrenoids also help to enhance photosynthesis under hyperoxia conditions, in addition to their role in the CCM.

Many questions remain to be answered to fully understand how hydrogen peroxide signalling leads to the formation of pyrenoids, regardless of whether low levels of inorganic carbon or hyperoxia are the eliciting cue. It is possible that other signals may affect the formation of pyrenoids, perhaps in response to other environmental stresses. Furthermore, how pyrenoids assemble and the specific roles of each of their different parts still remain to be explored. Nevertheless, the work of Neofotis et al. sets the scene for new, exciting avenues of research that may lead to the development of more efficient algae that can be used in bioreactors and other biotechnological applications.

References

Article and author information

Author details

  1. Britta Foerster

    Britta Foerster is in the Research School of Biology, Australian National University, Canberra, Australia

    For correspondence
    britta.forster@anu.edu.au
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5231-0954

Publication history

  1. Version of Record published: December 22, 2021 (version 1)

Copyright

© 2021, Foerster

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 522
    Page views
  • 48
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Biochemistry and Chemical Biology
    2. Cell Biology
    Thomas S McAlear, Susanne Bechstedt
    Research Article Updated

    Cells increase microtubule dynamics to make large rearrangements to their microtubule cytoskeleton during cell division. Changes in microtubule dynamics are essential for the formation and function of the mitotic spindle, and misregulation can lead to aneuploidy and cancer. Using in vitro reconstitution assays we show that the mitotic spindle protein Cytoskeleton-Associated Protein 2 (CKAP2) has a strong effect on nucleation of microtubules by lowering the critical tubulin concentration 100-fold. CKAP2 increases the apparent rate constant ka of microtubule growth by 50-fold and increases microtubule growth rates. In addition, CKAP2 strongly suppresses catastrophes. Our results identify CKAP2 as the most potent microtubule growth factor to date. These finding help explain CKAP2’s role as an important spindle protein, proliferation marker, and oncogene.

    1. Biochemistry and Chemical Biology
    2. Developmental Biology
    Lucas C Pantaleão et al.
    Research Article Updated

    Maternal obesity during pregnancy has immediate and long-term detrimental effects on the offspring heart. In this study, we characterized the cardiac and circulatory lipid profiles in late gestation E18.5 fetuses of diet-induced obese pregnant mice and established the changes in lipid abundance and fetal cardiac transcriptomics. We used untargeted and targeted lipidomics and transcriptomics to define changes in the serum and cardiac lipid composition and fatty acid metabolism in male and female fetuses. From these analyses we observed: (1) maternal obesity affects the maternal and fetal serum lipidome distinctly; (2) female fetal heart lipidomes are more sensitive to maternal obesity than males; (3) changes in lipid supply might contribute to early expression of lipolytic genes in mouse hearts exposed to maternal obesity. These results highlight the existence of sexually dimorphic responses of the fetal heart to the same in utero obesogenic environment and identify lipids species that might mediate programming of cardiovascular health.