The enigmatic loss of light‐independent chlorophyll biosynthesis from an Antarctic green alga in a light‐limited environment

Cvetkovska, Marina; Orgnero, Shane; Hüner, Norman P. A.; Smith, David Roy

doi:10.1111/nph.15623

Cited by 16 publications

(17 citation statements)

References 70 publications

(112 reference statements)

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“…Given these conditions, one might assume that being able to synthesize chlorophyll in the dark would be a major asset for an alga that calls Lake Bonney home. But recently, to our great surprise, we discovered that UWO241 has lost the ability to do just that, and we hypothesized that ICE-MDV has as well [9]. Here, we briefly update our findings, showing that our prediction for ICE-MDV was wrong, which may have implications for how we interpreted the loss of light-independent chlorophyll synthesis in UWO241.…”

Section: Main Documentmentioning

confidence: 62%

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Presence and absence of light-independent chlorophyll biosynthesis among Chlamydomonas green algae in an ice-covered Antarctic lake

Smith

Cvetkovska

Hüner

et al. 2019

Communicative & Integrative Biology

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The cold, permanently ice-covered waters of Lake Bonney, Antarctica, may seem like an uninviting place for an alga, but they are home to a diversity of photosynthetic life, including Chlamydomonas sp. UWO241, a psychrophile residing in the deep photic zone. Recently, we found that UWO241 has lost the genes responsible for light-independent chlorophyll biosynthesis, which is surprising given that this green alga comes from a light-limited environment and experiences extended periods of darkness during the Antarctic winter. Why discard such a process? We argued that it might be linked to the very high dissolved oxygen concentration of Lake Bonney at the depth at which UWO241 is found. Oxygen is the Achilles' heel of the key enzyme involved in light-independent chlorophyll biosynthesis: DPOR. If this hypothesis is true, then other algae in Lake Bonney should also be susceptible to losing DPOR, such as Chlamydomonas sp. ICE-MDV, which predominantly resides in the chemocline, a depth with an even higher oxygen concentration than that where UWO241 exists. Here, we report that, contrary to our earlier prediction, ICE-MDV has maintained the genes encoding DPOR. We briefly discuss the implications of this finding in relation to the loss of light-independent chlorophyll synthesis in UWO241. ARTICLE HISTORY

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Section: Main Documentmentioning

confidence: 62%

“…Chloroplast and nuclear genome sequencing demonstrated that UWO241 contains por but lacks chlB, chlL, and chlN, indicating it has discarded DPOR and is now entirely dependent on LPOR for making chlorophyll [9]. Why would any self-respecting photosynthesizer living in a light-limited environment dispose of DPOR?…”

Section: Main Documentmentioning

confidence: 99%

Presence and absence of light-independent chlorophyll biosynthesis among Chlamydomonas green algae in an ice-covered Antarctic lake

Smith

Cvetkovska

Hüner

et al. 2019

Communicative & Integrative Biology

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“…While most of the genes involved in Chl synthesis were downregulated and the Chl a pool per cell decreased in prolonged darkness ( Table S5, Figure S1F ), genes encoding protochlorophyllide reductase POR and magnesium chelatase H subunit were upregulated in darkness. As previously suggested ( 52 ), the duplication of protochlorophyllide reductase POR genes in microalgae might allow for neo-functionalization, which here could ensure a ready supply to convert protochlorophyllide into chlorophyll when light returns ( 53 ). While the maintenance of magnesium chelatase H subunit gene expression in prolonged darkness may also be involved in Chl production, this particular subunit is also known to contribute to retrograde chloroplast signaling.…”

Section: Discussionmentioning

confidence: 80%

Hypometabolism to survive the long polar night in the diatomFragilariopsis cylindrus

Joli

Concia

Mocaer

et al. 2023

Preprint

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Diatoms, the major eukaryotic phytoplankton in polar regions, are essential to sustain Arctic and Antarctic ecosystems. As such, it is fundamental to understand the physiological mechanisms and associated molecular basis of their resilience to the long polar night. Here, we report an integrative approach revealing that in prolonged darkness, diatom cells enter a state of quiescence associated with reduced metabolic and transcriptional activity during which no cell division occurs. We propose that minimal energy is provided by respiration and degradation of protein, carbohydrate, and lipid stores and that homeostasis is maintained by autophagy in prolonged darkness. We also report internal structural changes that manifest the morphological acclimation of cells to darkness. Our results further indicate that immediately following a return to light, diatom cells are able to use photoprotective mechanisms and rapidly resume photosynthesis. Cell division resumed rates similar to those before darkness. Our study demonstrates the remarkable robustness of polar diatoms to prolonged darkness at low temperatures.

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“…Oceanic diatoms Phaeodactylum tricornutum, Thalassiosira pseudonana and Nannochloropsis oceanica lost LIPOR because they are majorly present in Fe-sufficient oceanic water (Przybyla-Toscano et al, 2021). The low availability of micronutrient Fe encouraged the dispensability of LIPOR and the establishment of LPOR for better adaptability of other oceanic phototrophs that acquired LPOR by horizontal gene transfer (Behrenfeld et al, 2006;Bowler et al, 2010;Cvetkovska et al, 2019) The LPOR activity in different species is also temperature dependent. In Synechocystis the optimum LPOR activity is at 30 0 C. However, in thermophilic cyanobacterium Thermosynechococcus elongates the optimum temperature for LPOR activity is between 50 0 C-55 0 C and it is less active at room temperature (McFarlane et al, 2005).…”

Section: Impact Of Other Environmental Factors On Lpor Origin and Evo...mentioning

confidence: 99%

Fortuitous events in the evolution of Light-dependent Protochlorophyllide Oxidoreductase

Vedalankar

Tripathy

2023

Preprint

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Light-dependent protochlorophyllide oxidoreductase (LPOR) is a nuclear-encoded photoenzyme in many photosynthetic organisms. LPOR originated in primitive cyanobacterial ancestors during the great oxygenation event that was detrimental to the existence of the oxygen-sensitive LIPOR that prevailed in anoxygenic Earth. Both LIPOR and LPOR catalyse reduction of protochlorophyllide to chlorophyllide in the penultimate step of chlorophyll biosynthesis. Except for angiosperms and gnetophytes several oxygenic phototrophs harbour both LIPOR and LPOR. The coexistence of LIPOR and LPOR in certain phototrophs provides niche spaces for organisms in unconducive environment. The selection pressure of increased O2 concentration, changing light quality and quantity at different depths of the ocean, nutrient status of water, gene reorganization during several endosymbiotic events, horizontal gene transfer, LIPOR gene loss and multiple duplication events played a major role in the evolution and diversification of LPOR and its isoforms in photosynthetic and non-photosynthetic organisms. In the absence of LIPOR angiosperms become vulnerable to protochlorophyllide-sensitized and light-induced oxidative stress mediated by singlet oxygen. To overcome the photo-damage PORA was expressed abundantly in the plastids of etiolated plants. PORB evolved to take over the function of vanishing PORA isoform in light. Brassicales evolved PORC to protect plants from high light and other environmental stresses.

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The enigmatic loss of light‐independent chlorophyll biosynthesis from an Antarctic green alga in a light‐limited environment

Cited by 16 publications

References 70 publications

Presence and absence of light-independent chlorophyll biosynthesis among Chlamydomonas green algae in an ice-covered Antarctic lake

Presence and absence of light-independent chlorophyll biosynthesis among Chlamydomonas green algae in an ice-covered Antarctic lake

Hypometabolism to survive the long polar night in the diatomFragilariopsis cylindrus

Fortuitous events in the evolution of Light-dependent Protochlorophyllide Oxidoreductase

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