Concerted Up-regulation of Aldehyde/Alcohol Dehydrogenase (ADHE) and Starch in Chlamydomonas reinhardtii Increases Survival under Dark Anoxia

Lis, Robert van; Popek, Marion; Couté, Yohann; Kosta, Artémis; Drapier, Dominique; Nitschke, Wolfgang; Atteia, Ariane

doi:10.1074/jbc.m116.766048

Cited by 28 publications

(33 citation statements)

References 69 publications

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“…Only Gonium pectoral and Volvox species lack a functional METE gene (Helliwell et al, 2011) and thus depend on exogenous vitamin B12 scavenged from the environment or obtained via the establishment of beneficial interactions with bacteria. The secretion of potential carbon sources for nearby respiring prokaryotes in the form of organic compounds such as acetate, ethanol, and formate by C. reinhardtii at night (Yang et al, 2014;van Lis et al, 2017) also speaks to such an interaction.…”

Section: Ecologymentioning

confidence: 99%

A Series of Fortunate Events: Introducing Chlamydomonas as a Reference Organism

2019

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The unicellular alga Chlamydomonas reinhardtii is a classical reference organism for studying photosynthesis, chloroplast biology, cell cycle control, and cilia structure and function. It is also an emerging model for studying sensory cilia, the production of high-value bioproducts, and in situ structural determination. Much of the early appeal of Chlamydomonas was rooted in its promise as a genetic system, but like other classic model organisms, this rise to prominence predated the discovery of the structure of DNA, whole-genome sequences, and molecular techniques for gene manipulation. The haploid genome of C. reinhardtii facilitates genetic analyses and offers many of the advantages of microbial systems applied to a photosynthetic organism. C. reinhardtii has contributed to our understanding of chloroplast-based photosynthesis and cilia biology. Despite pervasive transgene silencing, technological advances have allowed researchers to address outstanding lines of inquiry in algal research. The most thoroughly studied unicellular alga, C. reinhardtii, is the current standard for algal research, and although genome editing is still far from efficient and routine, it nevertheless serves as a template for other algae. We present a historical retrospective of the rise of C. reinhardtii to illuminate its past and present. We also present resources for current and future scientists who may wish to expand their studies to the realm of microalgae. WHY ALGAE (IN GENERAL) AND CHLAMYDOMONAS (SPECIFICALLY)? Algae represent a very large and diverse polyphyletic group of photosynthetic eukaryotes (Blaby-Haas and Merchant, 2019). They occupy all possible ecological niches on the planet, and therefore constitute a potential reservoir of untapped functional capabilities for adaptation to the environment. Algae are primary producers that contribute ;50% of total carbon fixation worldwide (Field et al., 1998), which makes their study fundamental to our understanding of global primary production and carbon flux. They also offer a low-cost option for the large-scale production of high-value molecules, since algae only require water, salts, air, and light. Unicellular algae such as the ciliated green alga Chlamydomonas reinhardtii offer high signal-to-noise during experiments due to the ease of growth in controlled medium and environments (temperature and light regimes) and the homogenous nature of the cultures, and they grow much more rapidly than classic plant models. With its haploid genome, C. reinhardtii is well suited for classical genetics, as loss-of-function mutations are immediately expressed and more likely lead to observable phenotypes compared with diploid organisms. C. reinhardtii not only responds to light, but it also anticipates environmental transitions like dawn and dusk under the supervision of a circadian system, which coordinates cell division, photosynthesis, and cilia biogenesis, representing three fundamental research topics (Noordally and Millar, 2015). Other topics of research using C. reinhardtii include t...

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Section: Ecologymentioning

confidence: 99%

A Series of Fortunate Events: Introducing Chlamydomonas as a Reference Organism

2019

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“…AdhE converts acetyl-coenzyme A to acetaldehyde and then to ethanol, in a two-step reaction that is coupled with the oxidation of two NADH molecules into NAD + . The biochemistry of AdhE enzymatic activities is well characterized 2,3 . In particular, a lot of investigations looked into this key fermentative enzyme in order to engineer novel ethanol-producing bacteria 4,5 or identify bacterial strains capable of growing under ethanol 6 .…”

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confidence: 99%

“…These helical macromolecular assemblies were observed for the first time in the 70's in bacteria 12 . These filaments of AdhE are widely conserved in bacteria 13 and also in phylogenetically distant organisms such as Chlamydomonas reinhardtii 2 and Entamoeba histolytica 14 . While their wide conservation probably highlights an essential function, the exact role of AdhE filaments remains unknown.…”

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confidence: 99%

Filamentation of the bacterial bi-functional alcohol/aldehyde dehydrogenase AdhE is essential for substrate channeling and enzymatic regulation

Pony

Rapisarda

Terradot

et al. 2019

Preprint

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Acetaldehyde -alcohol dehydrogenase (AdhE) enzymes are a key metabolic enzyme in bacterial physiology and pathogenicity. They convert acetyl-CoA to ethanol via an acetaldehyde intermediate during ethanol fermentation in anaerobic environment. This twostep reaction is associated to NAD + regeneration, essential for glycolysis. The bifunctional AdhE enzyme is conserved in all bacterial kingdoms but also in more phylogenetically distant microorganisms such as green microalgae. In synthetic biology and biotechnology, because of its central role in bacterial alcoholic fermentation, AdhE raised a lot of attention as a key enzyme to produce ethanol from bacterial cultures.AdhE is commonly found as an oligomeric form called spirosomes. While these helical macromolecular assemblies are conserved, their function remains elusive. We used cryoelectron microscopy to obtain structures of Escherichia coli spirosomes in different conformational states. We confirm that spirosomes contain active AdhE monomers and show that AdhE filamentation is essential for its activity in vitro and function in vivo. The detailed analysis of these structures provides insight showing that AdhE filamentation is essential for substrate channeling within the filament and for the regulation of enzyme activity. These new data will help to design molecules or mutations that control AdhE activity to fight bacterial pathogens or to optimize ethanol production in biotechnology.

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“…Protein separation and immunoblot analyses were performed as described previously [24]. Proteins were separated on a 12% or a 8-13% [w/v] linear gradient SDS/ PAGE.…”

Section: Protein Gel Electrophoresis and Immunodetection Of Hcpsmentioning

confidence: 99%

“…Mass spectrometry (MS)-based proteomics identified the HCP2 isoform in mitochondria isolated from algal cells grown under mixotrophic conditions [21]. Pursuing our long-standing interest in the survival of C. reinhardtii in dark anoxia [22][23][24], we set up a multilevel approach to clarify the characteristics, relevance and role of its different HCPs. More specifically, we studied: (a) the structural and redox relatedness between the algal and the bacterial proteins, (b) the evolutionary origin of the algal HCPs, and (c) the physiological role of HCPs in the photosynthetic alga.…”

Section: Introductionmentioning

confidence: 99%

Hybrid cluster proteins in a photosynthetic microalga

et al. 2019

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Hybrid cluster proteins (HCPs) are metalloproteins characterized by the presence of an iron‐sulfur‐oxygen cluster. These proteins occur in all three domains of life. In eukaryotes, HCPs have so far been found only in a few anaerobic parasites and photosynthetic microalgae. With respect to all species harboring an HCP, the green microalga Chlamydomonas reinhardtii stands out by the presence of four HCP genes. The study of the gene and protein structures as well as the phylogenetic analyses strongly support a model in which the HCP family in the alga has emerged from a single gene of alpha proteobacterial origin and then expanded by several rounds of duplications. The spectra and redox properties of HCP1 and HCP3, produced heterologously in Escherichia coli, were analyzed by electron paramagnetic resonance spectroscopy on redox‐titrated samples. Both proteins contain a [4Fe‐4S]‐cluster as well as a [4Fe‐2O‐2S]‐hybrid cluster with paramagnetic properties related to those of HCPs from Desulfovibrio species. Immunoblotting experiments combined with mass spectrometry‐based proteomics showed that both nitrate and darkness contribute to the strong upregulation of the HCP levels in C. reinhardtii growing under oxic conditions. The link to the nitrate metabolism is discussed in the light of recent data on the potential role of HCP in S‐nitrosylation in bacteria.

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Concerted Up-regulation of Aldehyde/Alcohol Dehydrogenase (ADHE) and Starch in Chlamydomonas reinhardtii Increases Survival under Dark Anoxia

Cited by 28 publications

References 69 publications

A Series of Fortunate Events: Introducing Chlamydomonas as a Reference Organism

A Series of Fortunate Events: Introducing Chlamydomonas as a Reference Organism

Filamentation of the bacterial bi-functional alcohol/aldehyde dehydrogenase AdhE is essential for substrate channeling and enzymatic regulation

Hybrid cluster proteins in a photosynthetic microalga

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