Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum

Škodová-Sveráková, Ingrid; Záhonová, Kristína; Juricová, Valéria; Danchenko, Maksym; Moos, Martin; Baráth, Péter; Prokopchuk, Galina; Butenko, Anzhelika; Lukáčová, Veronika; Kohútová, Lenka; Bučková, Barbora; Horák, Aleš; Faktorová, Drahomíra; Horváth, Anton; Šimek, Petr; Lukeš, Julius

doi:10.1186/s12915-021-01186-y

Cited by 20 publications

(19 citation statements)

References 110 publications

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“…The predicted compartmentalization of glycolysis and gluconeogenesis in B. argentea suggests this adaptation could be widespread in microeukaryotes and may reflect convergent evolution associated with hypoxia tolerance (21,50). The electron transport system of B. argentea and N. stella appeared to be an integration of oxygen-dependent and nitrate-dependent metabolisms, likely reflecting adaptations to hypoxic and/or anoxic environments.…”

Section: Discussionmentioning

confidence: 95%

“…The predicted localization of the glyoxylate cycle to the peroxisomes of N. stella may represent an adaptation of protistan peroxisomes to use H 2 O 2 for lipid metabolism in the SBB chemocline. The predicted compartmentalization of glycolysis and gluconeogenesis in B. argentea suggests this adaptation could be widespread in microeukaryotes and may reflect convergent evolution associated with hypoxia tolerance (21, 50).…”

Section: Discussionmentioning

confidence: 99%

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Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Powers

Gomaa

Billings

et al. 2022

Preprint

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Certain benthic foraminifera are known to thrive in marine sediments with low oxygen or even without detectable oxygen. Potential survival avenues used by these supposedly aerobic protists include fermentation and anaerobic respiration, although details on their adaptive mechanisms remain somewhat elusive. To better understand the metabolic versatility of foraminifera, we studied two benthic species that thrive in oxygen-depleted marine sediments. Here we detail, via transcriptomics and metatranscriptomics, differential gene expression of Nonionella stella and Bolivina argentea, collected from Santa Barbara Basin, California, USA, in response to varied oxygenation and chemical amendments. Organelle-specific metabolic reconstructions revealed that these two species utilize adaptable mitochondrial and peroxisomal metabolism that reflect their differing lifestyles. N. stella, most abundant in anoxia and characterized by the lack of food vacuoles and the abundance of intracellular lipid droplets, was predicted to couple the putative peroxisomal beta-oxidation and glyoxylate cycle with a versatile electron transport system and a partial TCA cycle running in the reductive direction. In contrast, B. argentea, most abundant in hypoxia and contains food vacuoles, was predicted to utilize the putative peroxisomal gluconeogenesis and a full TCA cycle but lacks the expression of key beta-oxidation and glyoxylate cycle genes. These metabolic adaptations likely confer ecological success while encountering deoxygenation and illuminate the importance of metabolic modifications and interactions between mitochondria and peroxisomes in protists.ImportanceForaminiferan protists are nearly ubiquitous in today’s oceans and likely were major components of the Neoproterozoic protistan community. While largely considered aerobic, certain foraminifera demonstrate surprising adaptability to hypoxia and anoxia, contributing to biogeochemical cycling in benthic environments. The analyses of Rhizarian adaptive metabolism set the stage for studying other microeukaryotes under increasing ocean deoxygenation. Revealing the metabolic roles of foraminifera in anaerobic biogeochemical cycling should spur reassessments of existing paleoecological datasets as well as new perspectives on the metabolic evolution of eukaryotic cells.

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Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Powers

Gomaa

Billings

et al. 2022

Preprint

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“…Finally, a 50 ul aliquot of the supernatant was used for liquid chromatographic – high resolution mass spectrometric analysis (LC-HRMS). The LC-HRMS methods were described in detail earlier 109,110 . Briefly: A Q Exactive Plus Orbitrap mass spectrometer coupled with a Dionex Ultimate 3000 liquid chromatograph (all Thermo Fisher Scientific, San Jose, CA, USA) was used for profiling of haem biosynthesis intermediates .…”

Section: Methodsmentioning

confidence: 99%

“…Finally, a 50 ul aliquot of the supernatant was used for liquid chromatographichigh resolution mass spectrometric analysis (LC-HRMS). The LC-HRMS methods were described in detail earlier 109,110…”

Section: Metabolomic Analysis Of Haem Biosynthesis Intermediatesmentioning

confidence: 99%

Integrative assessment of the transcriptome and virome of the poultry red mite Dermanyssus gallinae

Ribeiro

Hartmann

Bartošová-Sojková

et al. 2022

Preprint

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Dermanyssus gallinae is a blood-feeding mite that parasitises on wild birds and farmed poultry. The D. gallinae mite has a short life cycle of fewer than two weeks from the egg to an egg-laying female. The remarkably swift processing of blood, together with the capacity to blood-feed in most developmental stages, makes this mite a highly debilitating pest. We have constructed developmental stage-specific transcriptomes, through Illumina RNA-seq, to mine the repertoire of protein-encoding mRNA transcripts, products of which participate in key processes that ensure the success of blood digestion, rapid ontogeny, and immunity. As a result of high reproductive capacity, the prevalence of D. gallinae in egg-producing poultry farms globally causes significant economic losses. Acaricides that are used to limit the reproduction of D. gallinae mites target cys-loop ion channels, which are widely shared across the phylogeny of invertebrates. To catalogue a comprehensive list of potential invertebrate-specific ion channels, we have constructed and analysed an additional RNA-seq library of D. gallinae micro-dissected midguts, a tissue with direct exposure to host blood and potential anti-parasitics. We phylogenetically defined groups of cys-loop proteins and probed their sensitivity to selected acaricides. Ultimately, we have catalogued all assembled transcripts and their expression values in a hyper-linked excel sheet with available sequences of individual contigs. The transcriptomic data were complemented by mass-spectrometry (MS)-based metabolite identification and by viability assays using selected inhibitors applied either by microinjection or through artificial membrane feeding. Additionally, we have described the RNA-virome of D. gallinae and identified a novel virus dubbed Red Mite Quaranjavirus 1.

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“…In searches, amino-acid sequences of known glycosomal proteins from different organisms provided queries to retrieve orthologues and paralogues from the following databases: TriTrypDB ( https://tritrypdb.org/tritrypdb/app ), AmoebaDB ( https://amoebadb.org/amoeba/app ), OrthoMCL DB ( https://orthomcl.org/orthomcl/app ), NCBI (National Center for Biotechnology Information, https://www.ncbi.nlm.nih.gov/ ) and DiscobaDB ( https://zenodo.org/record/5563074 ) ( Wheeler, 2021 ). Query sequences were adopted on a basis of glycosomal localisation from proteomic and genomic studies ( Colasante et al, 2006 , 2013 ; Güther et al, 2014 ; Morales et al, 2016 ; Acosta et al, 2019 ; Durrani et al, 2020 ; González-Robles et al, 2020 ; Quiñones et al, 2020 ; Jansen et al, 2021 ; Wheeler, 2021 ; Škodová-Sveráková et al, 2021 ) or the many biochemical and cell biological studies published previously. Sequence screening in DiscobaDB ( Wheeler, 2021 ) was done using Geneious Prime ® 2022.0.1 and BLASTp with default parameters.…”

Section: Introductionmentioning

confidence: 99%

Delineating transitions during the evolution of specialised peroxisomes: Glycosome formation in kinetoplastid and diplonemid protists

Andrade-Alviárez

Bonive-Boscan

Cáceres

et al. 2022

Front. Cell Dev. Biol.

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One peculiarity of protists belonging to classes Kinetoplastea and Diplonemea within the phylum Euglenozoa is compartmentalisation of most glycolytic enzymes within peroxisomes that are hence called glycosomes. This pathway is not sequestered in peroxisomes of the third Euglenozoan class, Euglenida. Previous analysis of well-studied kinetoplastids, the ‘TriTryps’ parasites Trypanosoma brucei, Trypanosoma cruzi and Leishmania spp., identified within glycosomes other metabolic processes usually not present in peroxisomes. In addition, trypanosomatid peroxins, i.e. proteins involved in biogenesis of these organelles, are divergent from human and yeast orthologues. In recent years, genomes, transcriptomes and proteomes for a variety of euglenozoans have become available. Here, we track the possible evolution of glycosomes by querying these databases, as well as the genome of Naegleria gruberi, a non-euglenozoan, which belongs to the same protist supergroup Discoba. We searched for orthologues of TriTryps proteins involved in glycosomal metabolism and biogenesis. Predicted cellular location(s) of each metabolic enzyme identified was inferred from presence or absence of peroxisomal-targeting signals. Combined with a survey of relevant literature, we refine extensively our previously postulated hypothesis about glycosome evolution. The data agree glycolysis was compartmentalised in a common ancestor of the kinetoplastids and diplonemids, yet additionally indicates most other processes found in glycosomes of extant trypanosomatids, but not in peroxisomes of other eukaryotes were either sequestered in this ancestor or shortly after separation of the two lineages. In contrast, peroxin divergence is evident in all euglenozoans. Following their gain of pathway complexity, subsequent evolution of peroxisome/glycosome function is complex. We hypothesize compartmentalisation in glycosomes of glycolytic enzymes, their cofactors and subsequently other metabolic enzymes provided selective advantage to kinetoplastids and diplonemids during their evolution in changing marine environments. We contend two specific properties derived from the ancestral peroxisomes were key: existence of nonselective pores for small solutes and the possibility of high turnover by pexophagy. Critically, such pores and pexophagy are characterised in extant trypanosomatids. Increasing amenability of free-living kinetoplastids and recently isolated diplonemids to experimental study means our hypothesis and interpretation of bioinformatic data are suited to experimental interrogation.

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Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum

Cited by 20 publications

References 110 publications

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Integrative assessment of the transcriptome and virome of the poultry red mite Dermanyssus gallinae

Delineating transitions during the evolution of specialised peroxisomes: Glycosome formation in kinetoplastid and diplonemid protists

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