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The green alga Zygogonium ericetorum (Zygnematophyceae, Charophyta) shows high iron and aluminium tolerance: protection mechanisms and photosynthetic performance.

ABSTRACT: Streptophyte green algae, ancestors of Embryophytes, occur frequently in terrestrial habitats being exposed to high light intensities, water scarcity and potentially toxic metal cations under acidic conditions. The filamentous Zygogonium ericetorum synthesizes a purple vacuolar ferrous pigment, which is lost after aplanospore formation. However, it is unknown whether this cellular reorganization also removes excessive iron from the protoplast and how Z. ericetorum copes with high concentrations of aluminium. Here we show that aplanospore formation shifts iron into the extracellular space of the algal filament. Upon germination of aplanospores, aluminium is bound in the parental cell wall. Both processes reduce iron and aluminium in unpigmented filaments. Comparison of the photosynthetic oxygen production in response to light and temperature gradients in two different Z. ericetorum strains from an Austrian alpine and a Scottish highland habitat revealed lower values in the latter strain. In contrast, the Scottish strain showed a higher optimum quantum yield of PSII during desiccation stress followed by rehydration. Furthermore, pigmented filaments of both strains exhibited a higher light and temperature dependent oxygen production when compared to the unpigmented phenotype. Our results demonstrate a high metal tolerance of Z. ericetorum, which is crucial for surviving in acidic terrestrial habitats.

SUBMITTER: Herburger K

PROVIDER: S-EPMC4909054 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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The green alga Zygogonium ericetorum (Zygnematophyceae, Charophyta) shows high iron and aluminium tolerance: protection mechanisms and photosynthetic performance.

Herburger Klaus K Remias Daniel D Holzinger Andreas A

FEMS microbiology ecology 20160512 8

Streptophyte green algae, ancestors of Embryophytes, occur frequently in terrestrial habitats being exposed to high light intensities, water scarcity and potentially toxic metal cations under acidic conditions. The filamentous Zygogonium ericetorum synthesizes a purple vacuolar ferrous pigment, which is lost after aplanospore formation. However, it is unknown whether this cellular reorganization also removes excessive iron from the protoplast and how Z. ericetorum copes with high concentrations ...[more]

PMID: 27178434

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Project description:Main conclusionThe basal streptophyte Klebsormidium and the advanced Zygnema show adaptation to terrestrialization. Differences are found in photoprotection and resistance to short-term light changes, but not in CO 2 acquisition. Streptophyte green algae colonized land about 450-500 million years ago giving origin to terrestrial plants. We aim to understand how their physiological adaptations are linked to the ecological conditions (light, water and CO2) characterizing modern terrestrial habitats. A new Klebsormidium isolate from a strongly acidic environment of a former copper mine (Schwarzwand, Austria) is investigated, in comparison to Klebsormidium cf. flaccidum and Zygnema sp. We show that these genera possess different photosynthetic traits and water requirements. Particularly, the Klebsormidium species displayed a higher photoprotection capacity, concluded from non-photochemical quenching (NPQ) and higher tolerance to high light intensity than Zygnema. However, Klebsormidium suffered from photoinhibition when the light intensity in the environment increased rapidly, indicating that NPQ is involved in photoprotection against strong and stable irradiance. Klebsormidium was also highly resistant to cellular water loss (dehydration) under low light. On the other hand, exposure to relatively high light intensity during dehydration caused a harmful over-reduction of the electron transport chain, leading to PSII damages and impairing the ability to recover after rehydration. Thus, we suggest that dehydration is a selective force shaping the adaptation of this species towards low light. Contrary to the photosynthetic characteristics, the inorganic carbon (C i ) acquisition was equivalent between Klebsormidium and Zygnema. Despite their different habitats and restriction to hydro-terrestrial environment, the three organisms showed similar use of CO2 and HCO3- as source of Ci for photosynthesis, pointing out a similar adaptation of their CO2-concentrating mechanisms to terrestrial life.

Project description:BackgroundPlastid electron transport systems are essential not only for photosynthesis but also for dissipating excess reducing power and sinking excess electrons generated by various redox reactions. Although numerous organisms with plastids have lost their photoautotrophic lifestyles, there is a spectrum of known functions of remnant plastids in non-photosynthetic algal/plant lineages; some of non-photosynthetic plastids still retain diverse metabolic pathways involving redox reactions while others, such as apicoplasts of apicomplexan parasites, possess highly reduced sets of functions. However, little is known about underlying mechanisms for redox homeostasis in functionally versatile non-photosynthetic plastids and thus about the reductive evolution of plastid electron transport systems.ResultsHere we demonstrated that the central component for plastid electron transport systems, plastoquinone/plastoquinol pool, is still retained in a novel strain of an obligate heterotrophic green alga lacking the photosynthesis-related thylakoid membrane complexes. Microscopic and genome analyses revealed that the Volvocales green alga, chlamydomonad sp. strain NrCl902, has non-photosynthetic plastids and a plastid DNA that carries no genes for the photosynthetic electron transport system. Transcriptome-based in silico prediction of the metabolic map followed by liquid chromatography analyses demonstrated carotenoid and plastoquinol synthesis, but no trace of chlorophyll pigments in the non-photosynthetic green alga. Transient RNA interference knockdown leads to suppression of plastoquinone/plastoquinol synthesis. The alga appears to possess genes for an electron sink system mediated by plastid terminal oxidase, plastoquinone/plastoquinol, and type II NADH dehydrogenase. Other non-photosynthetic algae/land plants also possess key genes for this system, suggesting a broad distribution of an electron sink system in non-photosynthetic plastids.ConclusionThe plastoquinone/plastoquinol pool and thus the involved electron transport systems reported herein might be retained for redox homeostasis and might represent an intermediate step towards a more reduced set of the electron transport system in many non-photosynthetic plastids. Our findings illuminate a broadly distributed but previously hidden step of reductive evolution of plastid electron transport systems after the loss of photosynthesis.

Dataset Information

The green alga Zygogonium ericetorum (Zygnematophyceae, Charophyta) shows high iron and aluminium tolerance: protection mechanisms and photosynthetic performance.

Publications

The green alga Zygogonium ericetorum (Zygnematophyceae, Charophyta) shows high iron and aluminium tolerance: protection mechanisms and photosynthetic performance.

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