Adaptation to life on land at high O₂via transition from ferredoxin-to NADH-dependent redox balance

Abstract

Pyruvate : ferredoxin oxidoreductase (PFO) and iron only hydrogenase ([Fe]-HYD) are common enzymes among eukaryotic microbes that inhabit anaerobic niches. Their function is to maintain redox balance by donating electrons from food oxidation via ferredoxin (Fd) to protons, generating H 2 as a waste product. Operating in series, they constitute a soluble electron transport chain of one-electron transfers between FeS clusters. They fulfil the same function—redox balance—served by two electron-transfers in the NADH- and O 2 -dependent respiratory chains of mitochondria. Although they possess O 2 -sensitive FeS clusters, PFO, Fd and [Fe]-HYD are also present among numerous algae that produce O 2 . The evolutionary persistence of these enzymes among eukaryotic aerobes is traditionally explained as adaptation to facultative anaerobic growth. Here, we show that algae express enzymes of anaerobic energy metabolism at ambient O 2 levels (21% v/v), Chlamydomonas reinhardtii expresses them with diurnal regulation. High O 2 environments arose on Earth only approximately 450 million years ago. Gene presence/absence and gene expression data indicate that during the transition to high O 2 environments and terrestrialization, diverse algal lineages retained enzymes of Fd-dependent one-electron-based redox balance, while the land plant and land animal lineages underwent irreversible specialization to redox balance involving the O 2 -insensitive two-electron carrier NADH.

Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments

“…N. stella and B. argentea express characteristic proteins for anaerobic energy metabolism including pyruvate-ferredoxin oxidoreductase (PFOR) and [FeFe]-hydrogenase ( 28 – 30 ) ( Fig. 2, A and B ).…”

Evidence for a Syncytial Origin of Eukaryotes from Ancestral State Reconstruction

“…In addition to having mitochondria, the first eukaryote was sexual and had meiotic recombination ( Speijer et al 2015 ; Fu et al 2019 ; Hofstatter and Lahr 2019 ). It is known that hydrogenosomes and mitosomes arose from mitochondria via respiratory chain loss and ecological specialization in several independent lineages ( Embley and Martin 2006 ; Müller et al 2012 ; Maciszewski and Karnkowska 2019 ; Gould et al 2019 ), that primary plastids arose once ( Sánchez-Baracaldo et al 2017 ) and that secondary plastids arose several times independently from eukaryotes containing a primary plastid ( Maciszewski and Karnkowska 2019 ; Keeling 2004 ; Gould et al 2008 ). Ancestral state reconstruction should map these traits accordingly.…”

Occurrence, Evolution and Specificities of Iron-Sulfur Proteins and Maturation Factors in Chloroplasts from Algae

“…Concerning Fe-S proteins, it appears that the living environment or ecological niche of some microalgae have a strong impact on some metabolic pathways. It has already been noticed that the progressive adaptation of the aquatic (and terrestrial) life at increasing O 2 concentrations was accompanied by several changes in terms of the oxido-reduction metabolism, such as the appearance of Fe-S cluster-free, oxygen-resistant proteins (whereas “ancestor” proteins had Fe-S clusters) or the transition from a ferredoxin to a NADPH- and flavin-dependent redox metabolism [ 141 ]. Still, despite possessing an O 2 -dependent energy metabolism, some microalgae such as C. reinhardtii , but not all, have retained a developed anaerobic energy metabolism to cope with anoxic/hypoxic conditions that relies on O 2 -sensitive Fe-S cluster containing-enzymes (Fe-Fe hydrogenases, PFO).…”