Abstract

Main conclusionThe basal streptophyteKlebsormidiumand the advancedZygnemashow adaptation to terrestrialization. Differences are found in photoprotection and resistance to short-term light changes, but not in CO2acquisition.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 (Ci) 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.

Highlights

  • Streptophyte green algae started land colonization about 450–500 million years ago (MYA) and this was an important step for the evolution of terrestrial plants (Becker and Marin 2009; Becker 2013)

  • The pioneering behaviour of streptophyte green algae during land colonization is still present in modern habitats where they are abundant in freshwater, hydro-terrestrial habitats (Zygnema; Holzinger and Pichrtova 2016) and biological soil crusts (Klebsormidium; Holzinger and Karsten 2013; Karsten and Holzinger 2014) worldwide, and where they contribute to important ecological roles as primary production, carbon and nitrogen biogeochemical cycles, and soil stabilization (Elbert et al 2012)

  • We investigated the eco-physiological traits that make Klebsormidium and Zygnema capable to successfully colonize terrestrial habitats

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Summary

Introduction

Streptophyte green algae started land colonization about 450–500 million years ago (MYA) and this was an important step for the evolution of terrestrial plants (Becker and Marin 2009; Becker 2013). The pioneering behaviour of streptophyte green algae during land colonization is still present in modern habitats where they are abundant in freshwater, hydro-terrestrial habitats (Zygnema; Holzinger and Pichrtova 2016) and biological soil crusts (Klebsormidium; Holzinger and Karsten 2013; Karsten and Holzinger 2014) worldwide, and where they contribute to important ecological roles as primary production, carbon and nitrogen biogeochemical cycles, and soil stabilization (Elbert et al 2012) Occurrence in these environments expose cells to various and extreme environmental conditions including long exposure to high light intensities and cellular water loss i.e., dehydration (Holzinger and Pichrtova 2016). Klebsormidium and Zygnema have been shown to have different NPQ kinetics that might confer a different sensitivity of their photosynthetic apparatus to high light environments (Gerotto and Morosinotto 2013)

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