@article {4935, title = {Sentinel protist taxa of the McMurdo Dry Valley lakes, Antarctica: A review}, journal = {Frontiers in Ecology and Evolution}, volume = {12}, year = {2024}, month = {03/2024}, pages = {1323472}, abstract = {

High-latitude meromictic lakes such as those in the Antarctic McMurdo Dry Valleys (MDV) harbor aquatic ecosystems dominated by the microbial loop. Within this habitat, which is limited year-round by light and nutrients, protists, or single celled eukaryotes, play outsized roles in the food web as the dominant primary producers and the apex predators. Thus, the MDV lake ecosystem represents an ideal system to study the role of sentinel protist taxa in carbon and nutrient cycling. The perennially ice-covered lakes are part of the McMurdo Long Term Ecological Research (McM LTER; mcmlter.org) established in 1993. In this review we will highlight the diversity and trophic roles of the MDV lake protist community and compare environmental factors driving spatiotemporal patterns in key protist taxa in two lakes within the McM LTER, Lakes Bonney and Fryxell. We will then discuss lessons learned from manipulated experiments on the impact of current and future climate-driven environmental change on sensitive protist taxa. Last, we will integrate knowledge gained from 25 years of lab-controlled experiments on key photosynthetic protists to extend our understanding of the function of these extremophiles within the MDV aquatic food webs. Our research group has studied the distribution and function of the MDV microbial community for nearly two decades, training the next generation of scientists to tackle future problems of these globally significant microbes. This review article will also highlight early career scientists who have contributed to this body of work and represent the future of scientific understanding in the Anthropocene.

}, keywords = {LTER-MCM, Antarctica, Disturbance, McMurdo Dry Valley lakes, phytoplankton, protist}, doi = {10.3389/fevo.2024.1323472}, url = {https://www.frontiersin.org/articles/10.3389/fevo.2024.1323472}, author = {Rachael M. Morgan-Kiss and Popson, Devon and Pereira, Rochelle and Dolhi-Binder, J and Teufel, Amber G. and Li, Wei and Kalra, Isha and Sherwell, Shasten S. and Reynebeau, Emily and Cristina D. Takacs-Vesbach} } @article {4937, title = {High salt-induced PSI-supercomplex is associated with high CEF and attenuation of state transitions}, journal = {Photosynthesis Research}, volume = {157}, year = {2023}, month = {09/2023}, pages = {65 - 84}, abstract = {

While PSI-driven cyclic electron flow (CEF) and assembly of thylakoid supercomplexes have been described in model organisms like Chlamydomonas reinhardtii, open questions remain regarding their contributions to survival under long-term stress. The Antarctic halophyte, C. priscuii UWO241 (UWO241), possesses constitutive high CEF rates and a stable PSI-supercomplex as a consequence of adaptation to permanent low temperatures and high salinity. To understand whether CEF represents a broader acclimation strategy to short- and long-term stress, we compared high salt acclimation between the halotolerant UWO241, the salt-sensitive model, C. reinhardtii, and a moderately halotolerant Antarctic green alga, C. sp. ICE-MDV (ICE-MDV). CEF was activated under high salt and associated with increased non-photochemical quenching in all three Chlamydomonas species. Furthermore, high salt-acclimated cells of either strain formed a PSI-supercomplex, while state transition capacity was attenuated. How the CEF-associated PSI-supercomplex interferes with state transition response is not yet known. We present a model for interaction between PSI-supercomplex formation, state transitions, and the important role of CEF for survival during long-term exposure to high salt.

}, keywords = {LTER-MCM, acclimation, Antarctica, Chlamydomonas, Cyclic electron flow, PSI-supercomplex, salinity, state transitions}, issn = {0166-8595}, doi = {10.1007/s11120-023-01032-y}, url = {https://link.springer.com/10.1007/s11120-023-01032-y}, author = {Kalra, Isha and Wang, Xin and Zhang, Ru and Rachael M. Morgan-Kiss} } @article {4814, title = {Antarctic lake phytoplankton and bacteria from near-surface waters exhibit high sensitivity to climate-driven disturbance}, journal = {Environmental Microbiology}, year = {2022}, month = {07/2022}, abstract = {

The McMurdo Dry Valleys (MDVs), Antarctica, represent a cold, desert ecosystem poised on the threshold of melting and freezing water. The MDVs have experienced dramatic signs of climatic change, most notably a warm austral summer in 2001\–2002 that caused widespread flooding, partial ice cover loss and lake level rise. To understand the impact of these climatic disturbances on lake microbial communities, we simulated lake level rise and ice-cover loss by transplanting dialysis-bagged communities from selected depths to other locations in the water column or to an open water perimeter moat. Bacteria and eukaryote communities residing in the surface waters (5 m) exhibited shifts in community composition when exposed to either disturbance, while microbial communities from below the surface were largely unaffected by the transplant. We also observed an accumulation of labile dissolved organic carbon in the transplanted surface communities. In addition, there were taxa-specific sensitivities: cryptophytes and Actinobacteria were highly sensitive particularly to the moat transplant, while chlorophytes and several bacterial taxa increased in relative abundance or were unaffected. Our results reveal that future climate-driven disturbances will likely undermine the stability and productivity of MDV lake phytoplankton and bacterial communities in the surface waters of this extreme environment.

}, keywords = {LTER-MCM}, doi = {10.1111/1462-2920.16113}, url = {https://onlinelibrary.wiley.com/doi/10.1111/1462-2920.16113}, author = {Sherwell, Shasten S. and Kalra, Isha and Li, Wei and Diane M. McKnight and John C. Priscu and Rachael M. Morgan-Kiss} } @article {4766, title = {Cyclic electron flow (CEF) and ascorbate pathway activity provide constitutive photoprotection for the photopsychrophile, Chlamydomonas sp. UWO 241~(renamed Chlamydomonas priscuii)}, journal = {Photosynthesis Research}, volume = {151}, year = {2022}, month = {03/2022}, pages = {235 - 250}, abstract = {

Under environmental stress, plants and algae employ a variety of strategies to protect the photosynthetic apparatus and maintain photostasis. To date, most studies on stress acclimation have focused on model organisms which possess limited to no tolerance to stressful extremes. We studied the ability of the Antarctic alga Chlamydomonas sp. UWO 241 (UWO 241) to acclimate to low temperature, high salinity or high light. UWO 241 maintained robust growth and photosynthetic activity at levels of temperature (2 \°C) and salinity (700 mM NaCl) which were nonpermissive for a mesophilic sister species, Chlamydomonas raudensis SAG 49.72 (SAG 49.72). Acclimation in the mesophile involved classic mechanisms, including downregulation of light harvesting and shifts in excitation energy between photosystem I and II. In contrast, UWO 241 exhibited high rates of PSI-driven cyclic electron flow (CEF) and a larger capacity for nonphotochemical quenching (NPQ). Furthermore, UWO 241 exhibited constitutively high activity of two key ascorbate cycle enzymes, ascorbate peroxidase and glutathione reductase and maintained a large ascorbate pool. These results matched the ability of the psychrophile to maintain low ROS under short-term photoinhibition conditions. We conclude that tight control over photostasis and ROS levels are essential for photosynthetic life to flourish in a native habitat of permanent photooxidative stress. We propose to rename this organism Chlamydomonas priscuii.

}, keywords = {LTER-MCM, Antarctica, ascorbate, Cyclic electron flow, Photosystem I, Psychrophile, ROS}, doi = {10.1007/s11120-021-00877-5}, url = {https://link.springer.com/article/10.1007/s11120-021-00877-5}, author = {Stahl-Rommel, Sarah and Kalra, Isha and D{\textquoteright}Silva, Susanna and Hahn, Mark M. and Popson, Devon and Cvetkovska, Marina and Rachael M. Morgan-Kiss} } @article {4716, title = {Photosynthetic adaptation to polar life: Energy balance, photoprotection and genetic redundancy}, journal = {Journal of Plant Physiology}, volume = {268}, year = {2022}, month = {01/2022}, pages = {153557}, abstract = {

The persistent low temperature that characterize polar habitats combined with the requirement for light for all photoautotrophs creates a conundrum. The absorption of too much light at low temperature can cause an energy imbalance that decreases photosynthetic performance that has a negative impact on growth and can affect long-term survival. The goal of this review is to survey the mechanism(s) by which polar photoautotrophs maintain cellular energy balance, that is, photostasis to overcome the potential for cellular energy imbalance in their low temperature environments. Photopsychrophiles are photosynthetic organisms that are obligately adapted to low temperature (0-15 \°C) but usually die at higher temperatures (\≥20 \°C). In contrast, photopsychrotolerant species can usually tolerate and survive a broad range of temperatures (5-40 \°C). First, we summarize the basic concepts of excess excitation energy, energy balance, photoprotection and photostasis and their importance to survival in polar habitats. Second, we compare the photoprotective mechanisms that underlie photostasis and survival in aquatic cyanobacteria and green algae as well as terrestrial Antarctic and Arctic plants. We show that polar photopsychrophilic and photopsychrotolerant organisms attain energy balance at low temperature either through a regulated reduction in the efficiency of light absorption or through enhanced capacity to consume photosynthetic electrons by the induction of O2\ as an alternative electron acceptor. Finally, we compare the published genomes of three photopsychrophilic and one photopsychrotolerant alga with five mesophilic green algae including the model green alga, Chlamydomonas reinhardtii. We relate our genomic analyses to photoprotective mechanisms that contribute to the potential attainment of photostasis. Finally, we discuss how the observed genomic redundancy in photopsychrophilic genomes may confer energy balance, photoprotection and resilience to their harsh polar environment. Primary production in aquatic, Antarctic and Arctic environments is dependent on diverse algal and cyanobacterial communities. Although mosses and lichens dominate the Antarctic terrestrial landscape, only two extant angiosperms exist in the Antarctic. The identification of a single \‘molecular key\’ to unravel adaptation of photopsychrophily and photopsychrotolerance remains elusive. Since these photoautotrophs represent excellent biomarkers to assess the impact of global warming on polar ecosystems, increased study of these polar photoautotrophs remains essential.

}, keywords = {LTER-MCM, genomic redundancy, light, photoprotection, photopsychrophily, photopsychrotolerance, Photosynthesis, temperature}, doi = {10.1016/j.jplph.2021.153557}, url = {https://www.sciencedirect.com/science/article/pii/S0176161721001966}, author = {H{\"u}ner, Norman P. A. and Smith, David R. and Cvetkovska, Marina and Zhang, Xi and Alexander G. Ivanov and Szyszka-Mroz, Beth and Kalra, Isha and Rachael M. Morgan-Kiss} } @phdthesis {4678, title = {Role of cyclic electron flow (CEF) and photosystem I (PSI) supercomplex formation during acclimation to long-term salinity stress in green algae: A comparative study}, volume = {PhD}, year = {2021}, month = {2021}, pages = {236}, school = {Miami University}, type = {Doctoral}, address = {Oxford, OH}, abstract = {Photosynthesis is one of the most important processes on Earth by which organisms convert solar energy into usable forms of energy. Linear electron flow (LEF) and cyclic electron flow (CEF) constitute two major pathways in photosynthesis. While LEF leads to production of both ATP and NADPH, CEF only produces ATP that helps balance the ATP:NADPH ratio required for carbon fixation. CEF also plays a major role during acclimation to several environmental stressors. However, the regulation and mechanism by which CEF operates is still not clearly understood. Recent studies have shown that formation of a protein supercomplex with PSI appears to be essential for induction of CEF in several model organisms. However, both supercomplex formation and CEF induction have been mainly studied under short-term, transitory stress conditions. In addition, the role and mechanism by which organisms may rely on CEF to survive in their natural habitat and acclimate to stress over a long period of time has not been considered. In this study we compared how three photosynthetic organisms (one model alga, Chlamydomonas reinhardtii; two extremophiles, C. sp. UWO241 and C. sp. ICE-MDV) utilize CEF to cope with their natural environment and adapt to steady-state environmental stress. To that end, the objectives of this thesis were i) to elucidate the role of CEF in long-term salinity acclimation ii) to understand the downstream changes associated with increased CEF, and iii) to identify whether PSI-supercomplexes are associated with increased CEF during salinity acclimation. We hypothesized that a stable PSI-supercomplex is required for high CEF, which in turn supports strong carbon fixation capacity for production of downstream metabolic products important for long-term acclimation to salinity stress. We showed for the first time, that increased CEF in UWO241 leads to excess ATP production and rewiring of downstream metabolism under high salinity. Next, we showed that a laboratory evolved salinity-tolerant strain of model C. reinhardtii uses constitutive upregulation of CEF to deal with salinity stress, which is in-turn associated with increased non-photochemical quenching and rewired carbon metabolism. Last, we show that CEF is involved in salinity acclimation in all three Chlamydomonas species, regardless of their salinity tolerance. We also show that PSI-supercomplexes are associated with increased CEF in these species. Characterization of high-salt supercomplex of C. reinhardtii revealed that it shares many similarities with the extensively described state 2 supercomplex, and that supercomplex composition might be species dependent rather than stress dependent.}, keywords = {LTER-MCM, acclimation, CEF, extremophile, Photosynthesis, salinity stress, supercomplex}, url = {https://www.proquest.com/docview/2572560585}, author = {Kalra, Isha}, editor = {Rachael M. Morgan-Kiss} } @article {4419, title = {Chlamydomonas sp. UWO 241 exhibits high cyclic electron flow and rewired metabolism under high salinity}, journal = {Plant Physiology}, year = {2020}, month = {03/2020}, abstract = {

The Antarctic green alga Chlamydomonas sp. UWO 241 (UWO 241) is adapted to permanent low temperatures, hypersalinity, and extreme shade. one of the most striking phenotypes of UWO 241 is an altered photosystem I (PSI) organization and constitutive PSI cyclic electron flow (CEF). To date, little attention has been paid to CEF during long-term stress acclimation, and the consequences of sustained CEF in UWO 241 are not known. In this study, we combined photobiology, proteomics, and metabolomics to understand the underlying role of sustained CEF in high salinity stress acclimation. High salt-grown UWO 241 exhibited increased thylakoid proton motive flux and an increased capacity for non-photochemical quenching. Under high salt, a significant proportion of the upregulated enzymes were associated with the Calvin Benson Bassham Cycle, carbon storage metabolism, and protein translation. Two key enzymes of the Shikimate pathway, DAHP synthase and chorismate synthase, were also upregulated, as well as indole-3-glycerol phosphate synthase, an enzyme involved in the biosynthesis of L-tryptophan and indole acetic acid. In addition, several compatible solutes (glycerol, proline, and sucrose) accumulated to high levels in high salt-grown UWO 241 cultures. We suggest that UWO 241 maintains constitutively high CEF through the associated PSI-cytochrome b6f supercomplex to support robust growth and strong photosynthetic capacity under a constant growth regime of low temperatures and high salinity.

}, keywords = {LTER-MCM}, doi = {10.1104/pp.19.01280}, url = {http://www.plantphysiol.org/content/early/2020/04/03/pp.19.01280}, author = {Kalra, Isha and Wang, Xin and Cvetkovska, Marina and Jeong, Jooyeon and McHargue, William and Zhang, Ru and H{\"u}ner, Norman and Yuan, Joshua S. and Rachael M. Morgan-Kiss} } @article {4154, title = {The Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of photosystem I in response to iron}, journal = {Photosynthesis Research}, volume = {9}, year = {2019}, month = {02/2019}, abstract = {

Chlamydomonas sp. UWO241 is a psychrophilic alga isolated from the deep photic zone of a perennially ice-covered Antarctic lake (east lobe Lake Bonney, ELB). Past studies have shown that C. sp. UWO241 exhibits constitutive downregulation of photosystem I (PSI) and high rates of PSI-associated cyclic electron flow (CEF). Iron levels in ELB are in the nanomolar range leading us to hypothesize that the unusual PSI phenotype of C. sp. UWO241 could be a response to chronic Fe-deficiency. We studied the impact of Fe availability in C. sp. UWO241, a mesophile, C. reinhardtii SAG11-32c, as well as a psychrophile isolated from the shallow photic zone of ELB, Chlamydomonas sp. ICE-MDV. Under Fe-deficiency, PsaA abundance and levels of photooxidizable P700 (ΔA820/A820) were reduced in both psychrophiles relative to the mesophile. Upon increasing Fe, C. sp. ICE-MDV and C. reinhardtii exhibited restoration of PSI function, while C. sp. UWO241 exhibited only moderate changes in PSI activity and lacked almost all LHCI proteins. Relative to Fe-excess conditions (200 μM Fe2+), C. sp. UWO241 grown in 18 μM Fe2+ exhibited downregulation of light harvesting and photosystem core proteins, as well as upregulation of a bestrophin-like anion channel protein and two CEF-associated proteins (NdsS, PGL1). Key enzymes of starch synthesis and shikimate biosynthesis were also upregulated. We conclude that in response to variable Fe availability, the psychrophile C. sp. UWO241 exhibits physiological plasticity which includes restructuring of the photo-chemical apparatus, increased PSI-associated CEF, and shifts in downstream carbon metabolism toward storage carbon and secondary stress metabolites.

}, keywords = {LTER-MCM, Antarctica, Cyclic electron flow, Iron, Photosystem I, Psychrophile}, issn = {0166-8595}, doi = {10.1007/s11120-019-00621-0}, url = {https://link.springer.com/article/10.1007/s11120-019-00621-0}, author = {Cook, Greg and Teufel, Amber and Kalra, Isha and Li, Wei and Wang, Xin and John C. Priscu and Rachael M. Morgan-Kiss} }