An official website of the United States government
Although cyanobacteria and algae represent a small fraction of the biomass of all primary producers, their photosynthetic activity accounts for roughly half of the daily CO2 fixation that occurs on Earth. These microorganisms are able to accomplish this feat by enhancing the activity of the CO2-fixing enzyme Rubisco using biophysical CO2 concentrating mechanisms (CCMs). Biophysical CCMs operate by concentrating bicarbonate and converting it into CO2 in a compartment that houses Rubisco (in contrast with other CCMs that concentrate CO2 via an organic intermediate, such as malate in the case of C4 CCMs). This activity provides Rubisco with a high concentration of its substrate, thereby increasing its reaction rate. The genetic engineering of a biophysical CCM into land plants is being pursued as a strategy to increase crop yields. This review focuses on the progress toward understanding the molecular components of cyanobacterial and algal CCMs, as well as recent advances toward engineering these components into land plants.
more »
« less
Carbon‐concentrating mechanisms are a key trait in lichen ecology and distribution
Abstract Carbon‐concentrating mechanisms (CCMs) are a widespread phenomenon in photosynthetic organisms. In vascular plants, the evolution of CCMs ([C44‐carbon compound] and crassulacean acid metabolism [CAM]) is associated with significant shifts, most often to hot, dry and bright, or aquatic environments. If and how CCMs drive distributions of other terrestrial photosynthetic organisms, remains little studied. Lichens are ecologically important obligate symbioses between fungi and photosynthetic organisms. The primary photosynthetic partner in these symbioses can include CCM‐presenting cyanobacteria (as carboxysomes), CCM‐presenting green algae (as pyrenoids) or green algae lacking any CCM. We use an extensive dataset of lichen communities from eastern North America, spanning a wide climatic range, to test the importance of CCMs as predictors of lichen ecology and distribution. We show that the presence or absence of CCMs leads to opposite responses to temperature and precipitation in green algal lichens, and different responses in cyanobacterial lichens. These responses contrast with our understanding of lichen physiology, whereby CCMs mitigate carbon limitation by water saturation at the cost of efficient use of vapor hydration. This study demonstrates that CCM status is a key functional trait in obligate lichen symbioses, equivalent in importance to its role in vascular plants, and central for studying present and future climate responses.
more »
« less
- Award ID(s):
- 2115190
- PAR ID:
- 10402138
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 104
- Issue:
- 5
- ISSN:
- 0012-9658
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Lichen thalli are formed through the symbiotic association of a filamentous fungus and photosynthetic green alga and/or cyanobacterium. Recent studies have revealed lichens also host highly diverse communities of secondary fungal and bacterial symbionts, yet few studies have examined the viral component within these complex symbioses. Here, we describe viral biodiversity and functions in cyanolichens collected from across North America and Europe. As current machine-learning viral-detection tools are not trained on complex eukaryotic metagenomes, we first developed efficient methods to remove eukaryotic reads prior to viral detection and a custom pipeline to validate viral contigs predicted with three machine-learning methods. Our resulting high-quality viral data illustrate that every cyanolichen thallus contains diverse viruses that are distinct from viruses in other terrestrial ecosystems. In addition to cyanobacteria, predicted viral hosts include other lichen-associated bacterial lineages and algae, although a large fraction of viral contigs had no host prediction. Functional annotation of cyanolichen viral sequences predicts numerous viral-encoded auxiliary metabolic genes (AMGs) involved in amino acid, nucleotide, and carbohydrate metabolism, including AMGs for secondary metabolism (antibiotics and antimicrobials) and fatty acid biosynthesis. Overall, the diversity of cyanolichen AMGs suggests that viruses may alter microbial interactions within these complex symbiotic assemblages.more » « less
-
Abstract Many photosynthetic species have evolved CO2-concentrating mechanisms (CCMs) to improve the efficiency of CO2 assimilation by Rubisco and reduce the negative impacts of photorespiration. However, the majority of plants (i.e. C3 plants) lack an active CCM. Thus, engineering a functional heterologous CCM into important C3 crops, such as rice (Oryza sativa) and wheat (Triticum aestivum), has become a key strategic ambition to enhance yield potential. Here, we review recent advances in our understanding of the pyrenoid-based CCM in the model green alga Chlamydomonas reinhardtii and engineering progress in C3 plants. We also discuss recent modeling work that has provided insights into the potential advantages of Rubisco condensation within the pyrenoid and the energetic costs of the Chlamydomonas CCM, which, together, will help to better guide future engineering approaches. Key findings include the potential benefits of Rubisco condensation for carboxylation efficiency and the need for a diffusional barrier around the pyrenoid matrix. We discuss a minimal set of components for the CCM to function and that active bicarbonate import into the chloroplast stroma may not be necessary for a functional pyrenoid-based CCM in planta. Thus, the roadmap for building a pyrenoid-based CCM into plant chloroplasts to enhance the efficiency of photosynthesis now appears clearer with new challenges and opportunities.more » « less
-
null (Ed.)Many photosynthetic organisms employ a CO 2 concentrating mechanism (CCM) to increase the rate of CO 2 fixation via the Calvin cycle. CCMs catalyze ≈50% of global photosynthesis, yet it remains unclear which genes and proteins are required to produce this complex adaptation. We describe the construction of a functional CCM in a non-native host, achieved by expressing genes from an autotrophic bacterium in an Escherichia coli strain engineered to depend on rubisco carboxylation for growth. Expression of 20 CCM genes enabled E. coli to grow by fixing CO 2 from ambient air into biomass, with growth in ambient air depending on the components of the CCM. Bacterial CCMs are therefore genetically compact and readily transplanted, rationalizing their presence in diverse bacteria. Reconstitution enabled genetic experiments refining our understanding of the CCM, thereby laying the groundwork for deeper study and engineering of the cell biology supporting CO 2 assimilation in diverse organisms.more » « less
-
The upside-down jellyfish, Cassiopea spp., host their algal symbionts inside a subset of amoebocytes, phagocytic cells that also play innate immune functions akin to macrophages from vertebrate animals. Amoebocyte precursors phagocytose algae from the jellyfish gut and store them inside intracellular compartments called symbiosomes. Subsequently, the precursors migrate to the mesoglea, differentiate into symbiotic amoebocytes, and roam throughout the jellyfish body where the algae remain photosynthetically active and supply the jellyfish host with a significant portion of their organic carbon needs. Here, we show that the amoebocyte symbiosome membrane contains V-H+-ATPase (VHA), the proton pump that acidifies phagosomes and lysosomes in all eukaryotes. Many symbiotic amoebocytes also abundantly express a carbonic anhydrase (CA), an enzyme that reversibly hydrates CO2 into H+ and HCO3−. Moreover, we found that the symbiosome lumen is pronouncedly acidic and that pharmacological inhibition of VHA or CA activities significantly decreases photosynthetic oxygen production in live jellyfish. These results point to a carbon concentrating mechanism (CCM) that co-opts VHA and CA from the phago-lysosomal machinery that ubiquitously mediates food digestion and innate immune responses. Analogous VHA-dependent CCMs have been previously described in reef-building corals, anemones, and giant clams; however, these other two cnidarians host their dinoflagellate algae inside gastrodermal cells -not in amoebocytes- and the clam hosts theirs within the gut lumen. Thus, our study identifies an example of convergent evolution at the cellular level that might broadly apply to invertebrate-microbe photosymbioses while also providing evolutionary links with intra- and extracellular food digestion and the immune system.more » « less
