Title: 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.
Lendemer, James C.; Keepers, Kyle G.; Tripp, Erin A.; Pogoda, Cloe S.; McCain, Christy M.; Kane, Nolan C.(
, American Journal of Botany)
Premise
Lichens are fungi that enter into obligate symbioses with photosynthesizing organisms (algae, cyanobacteria). Traditional narratives of lichens as binary symbiont pairs have given way to their recognition as dynamic metacommunities. Basidiomycete yeasts, particularly of the genusCyphobasidium, have been inferred to be widespread and important components of lichen metacommunities. Yet, the presence of basidiomycete yeasts across a wide diversity of lichen lineages has not previously been tested.
Methods
We searched for lichen‐associated cystobasidiomycete yeasts in newly generated metagenomic data from 413 samples of 339 lichen species spanning 57 families and 25 orders. The data set was generated as part of a large‐scale project to study lichen biodiversity gradients in the southern Appalachian Mountains Biodiversity Hotspot of southeastern North America.
Results
Our efforts detected cystobasidiomycete yeasts in nine taxa (Bryoria nadvornikiana,Heterodermia leucomelos,Lecidea roseotincta,Opegrapha vulgata,Parmotrema hypotropum,P. subsumptum,Usnea cornuta,U. strigosa, andU. subgracilis), representing 2.7% of all species sampled. Seven of these taxa (78%) are foliose (leaf‐like) or fruticose (shrubby) lichens that belong to families where basidiomycete yeasts have been previously detected. In several of the nine cases, cystobasidiomycete rDNA coverage was comparable to, or greater than, that of the primary lichen fungus single‐copy nuclear genomic rDNA, suggesting sampling artifacts are unlikely to account for our results.
Conclusions
Studies from diverse areas of the natural sciences have led to the need to reconceptualize lichens as dynamic metacommunities. However, our failure to detect cystobasidiomycetes in 97.3% (330 species) of the sampled species suggests that basidiomycete yeasts are not ubiquitous in lichens.
Allen, Jessica; McMullin, R. Troy(
, Biodiversity Information Science and Standards)
Community science-generated biodiversity data can provide essential information for understanding species distributions, behaviors and conservation statuses. However, their utility can be limited due to high uncertainty and variability in quality, especially for small taxonomically difficult organisms like fungi and insects. One important set of community-generated data that are increasingly used by scientists are Research Grade (RG) iNaturalist observations. These observations are aggregated into the Global Biodiversity Information Facility database. Here we assessed the accuracy of RG lichen observations in iNaturalist. Lichens are mutualistic symbioses formed between fungi and a photosynthetic partner, either algae or cyanobacteria that occur in every terrestrial ecosystem on the planet (Brodo et al. 2001). They are sensitive indicators of environmental health, especially air quality, and provide essental food and nesting material for animals, along with performing many other ecosystem services (Allen and Lendemer 2021, Brodo et al. 2001, Nimis et al. 2002). We examined hundreds of observations and determined if the identification was correct, if it was not possible to identify the observation given the data provided, or if the identification was incorrect. Identification accuracy of selected species varied widely, from zero observations with enough information for correct identification (e.g., Rhizocarpon geographicum and Cladonia chlorophaea ) to 100% correct identifications (e.g., Cetradonia linearis and Physconia subpallida , McMullin and Allen 2022). Most frequently, species that require microscopic examination or chemical tests for accurate identification were unable to be verified versus those that require only macromorphology. We provide a series of suggestions for best practices to improve the quality of RG observations and thus the utility of community-generated observation data for taxonomically difficult organisms.
Havrilla, Caroline A.; Chaudhary, V. Bala; Ferrenberg, Scott; Antoninka, Anita J.; Belnap, Jayne; Bowker, Matthew A.; Eldridge, David J.; Faist, Akasha M.; Huber‐Sannwald, Elisabeth; Leslie, Alexander D.; et al(
, Journal of Ecology)
Abstract
Understanding the importance of biotic interactions in driving the distribution and abundance of species is a central goal of plant ecology. Early vascular plants likely colonized land occupied by biocrusts — photoautotrophic, surface‐dwelling soil communities comprised of cyanobacteria, bryophytes, lichens and fungi — suggesting biotic interactions between biocrusts and plants have been at play for some 2,000 million years. Today, biocrusts coexist with plants in dryland ecosystems worldwide, and have been shown to both facilitate or inhibit plant species performance depending on ecological context. Yet, the factors that drive the direction and magnitude of these effects remain largely unknown.
We conducted a meta‐analysis of plant responses to biocrusts using a global dataset encompassing 1,004 studies from six continents.
Meta‐analysis revealed there is no simple positive or negative effect of biocrusts on plants. Rather, plant responses differ by biocrust composition and plant species traits and vary across plant ontogeny. Moss‐dominated biocrusts facilitated, while lichen‐dominated biocrusts inhibited overall plant performance. Plant responses also varied among plant functional groups: C4grasses received greater benefits from biocrusts compared to C3grasses, and plants without N‐fixing symbionts responded more positively to biocrusts than plants with N‐fixing symbionts. Biocrusts decreased germination but facilitated growth of non‐native plant species.
Synthesis. Results suggest that interspecific variation in plant responses to biocrusts, contingent on biocrust type, plant traits, and ontogeny can have strong impacts on plant species performance. These findings have important implications for understanding biocrust contributions to plant productivity and community assembly processes in ecosystems worldwide.
Hennacy, Jessica H; Jonikas, Martin C(
, Annual review of plant biology)
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.
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.
Koch, Natália M., Lendemer, James C., Manzitto‐Tripp, Erin A., McCain, Christy, and Stanton, Daniel E. Carbon‐concentrating mechanisms are a key trait in lichen ecology and distribution. Ecology 104.5 Web. doi:10.1002/ecy.4011.
Koch, Natália M., Lendemer, James C., Manzitto‐Tripp, Erin A., McCain, Christy, & Stanton, Daniel E. Carbon‐concentrating mechanisms are a key trait in lichen ecology and distribution. Ecology, 104 (5). https://doi.org/10.1002/ecy.4011
Koch, Natália M., Lendemer, James C., Manzitto‐Tripp, Erin A., McCain, Christy, and Stanton, Daniel E.
"Carbon‐concentrating mechanisms are a key trait in lichen ecology and distribution". Ecology 104 (5). Country unknown/Code not available: Wiley Blackwell (John Wiley & Sons). https://doi.org/10.1002/ecy.4011.https://par.nsf.gov/biblio/10402138.
@article{osti_10402138,
place = {Country unknown/Code not available},
title = {Carbon‐concentrating mechanisms are a key trait in lichen ecology and distribution},
url = {https://par.nsf.gov/biblio/10402138},
DOI = {10.1002/ecy.4011},
abstractNote = {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.},
journal = {Ecology},
volume = {104},
number = {5},
publisher = {Wiley Blackwell (John Wiley & Sons)},
author = {Koch, Natália M. and Lendemer, James C. and Manzitto‐Tripp, Erin A. and McCain, Christy and Stanton, Daniel E.},
}
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