Submergence of the filamentous Zygnematophyceae Mougeotia induces differential gene expression patterns associated with core metabolism and photosynthesis

The streptophyte algal class Zygnematophyceae is the closest algal sister lineage to land plants. In nature, Zygnematophyceae can grow in both terrestrial and freshwater habitats and how they do this is an important unanswered question. Here, we studied what happens to the zygnematophyceaen alga Mougeotia sp., which usually occurs in permanent and temporary freshwater bodies, when it is shifted to liquid growth conditions after growth on a solid substrate. Using global differential gene expression profiling, we identified changes in the core metabolism of the organism interlinked with photosynthesis; the latter went hand in hand with measurable impact on the photophysiology as assessed via pulse amplitude modulation (PAM) fluorometry. Our data reveal a pronounced change in the overall physiology of the alga after submergence and pinpoint candidate genes that play a role. These results provide insight into the importance of photophysiological readjustment when filamentous Zygnematophyceae transition between terrestrial and aquatic habitats.

Predicting Lifestyle from Positive Selection Data and Genome Properties in Oomycetes

As evidenced in parasitism, host and niche shifts are a source of genomic and phenotypic diversification. Exemplary is a reduction in the core metabolism as parasites adapt to a particular host, while the accessory genome often maintains a high degree of diversification. However, selective pressures acting on the genome of organisms that have undergone recent lifestyle or host changes have not been fully investigated. Here, we developed a comparative genomics approach to study underlying adaptive trends in oomycetes, a eukaryotic phylum with a wide and diverse range of economically important plant and animal parasitic lifestyles. Our analysis reveals converging evolution on biological processes for oomycetes that have similar lifestyles. Moreover, we find that certain functions, in particular carbohydrate metabolism, transport, and signaling, are important for host and environmental adaptation in oomycetes. Given the high correlation between lifestyle and genome properties in our oomycete dataset, together with the known convergent evolution of fungal and oomycete genomes, we developed a model that predicts plant pathogenic lifestyles with high accuracy based on functional annotations. These insights into how selective pressures correlate with lifestyle may be crucial to better understand host/lifestyle shifts and their impact on the genome.

Heterotrophic euglenid Rhabdomonas costata resembles its phototrophic relatives in many aspects of molecular and cell biology

Euglenids represent a group of protists with diverse modes of feeding. To date, only a partial genomic sequence of Euglena gracilis and transcriptomes of several phototrophic and secondarily osmotrophic species are available, while primarily heterotrophic euglenids are seriously undersampled. In this work, we begin to fill this gap by presenting genomic and transcriptomic drafts of a primary osmotroph, Rhabdomonas costata. The current genomic assembly length of 100 Mbp is 14× smaller than that of E. gracilis. Despite being too fragmented for comprehensive gene prediction it provided fragments of the mitochondrial genome and comparison of the transcriptomic and genomic data revealed features of its introns, including several candidates for nonconventional types. A set of 39,456 putative R. costata proteins was predicted from the transcriptome. Annotation of the mitochondrial core metabolism provides the first data on the facultatively anaerobic mitochondrion of R. costata, which in most respects resembles the mitochondrion of E. gracilis with a certain level of streamlining. R. costata can synthetise thiamine by enzymes of heterogenous provenances and haem by a mitochondrial-cytoplasmic C4 pathway with enzymes orthologous to those found in E. gracilis. The low percentage of green algae-affiliated genes supports the ancestrally osmotrophic status of this species.

Unique metabolic strategies in Hadean analogues reveal hints for primordial physiology

Primordial microorganisms are postulated to have emerged in H2-rich alkaline Hadean serpentinite-hosted environments with homoacetogenesis as a core metabolism. However, investigation of two modern serpentinization-active analogues of early Earth reveals that conventional H2-/CO2-dependent homoacetogenesis is thermodynamically unfavorable in situ due to picomolar CO2 levels. Through metagenomics and thermodynamics, we discover unique taxa capable of metabolism adapted to the habitat. This included a novel deep-branching phylum, "Ca. Lithoacetigenota", that exclusively inhabits Hadean analogues and harbors genes encoding alternative modes of H2-utilizing lithotrophy. Rather than CO2, these metabolisms utilize reduced carbon compounds detected in situ presumably serpentinization-derived: formate and glycine. The former employs a partial homoacetogenesis pathway and the latter a distinct pathway mediated by a rare selenoprotein - the glycine reductase. A survey of serpentinite-hosted system microbiomes shows that glycine reductases are diverse and nearly ubiquitous in Hadean analogues. "Ca. Lithoacetigenota" glycine reductases represent a basal lineage, suggesting that catabolic glycine reduction is an ancient bacterial innovation for gaining energy from geogenic H2 even under serpentinization-associated hyperalkaline, CO2-poor conditions. This draws remarkable parallels with ancestral archaeal H2-driven methyl-reducing methanogenesis recently proposed. Unique non-CO2-reducing metabolic strategies presented here may provide a new view into metabolisms that supported primordial life and the diversification of LUCA towards Archaea and Bacteria.

Recoding enhances the metabolic capabilities of two novel methylotrophic Asgardarchaeota lineages

Asgardarchaeota have been proposed as the closest living relatives to eukaryotes, and a total of 72 metagenome-assembled genomes (MAGs) representing six primary lineages in this archaeal phylum have thus far been described. These organisms are predicted to be fermentative organoheterotrophs contributing to carbon cycling in sediment ecosystems. Here, we double the genomic catalogue of Asgardarchaeota by obtaining 71 MAGs from a range of habitats around the globe, including deep subsurface, shallow lake, and geothermal spring sediments. Phylogenomic inferences followed by taxonomic rank normalisation confirmed previously established Asgardarchaeota classes and revealed four novel lineages, two of which were consistently recovered as monophyletic classes. We therefore propose the names Candidatus Hodarchaeia class nov. and Cand. Jordarchaeia class nov., derived from the gods Hod and Jord in Norse mythology. Metabolic inference suggests that both novel classes represent methylotrophic acetogens, encoding the transfer of methyl groups, such as methylated amines, to coenzyme M with acetate as the end product in remnants of a methanogen-derived core metabolism. This inferred mode of energy conservation is predicted to be enhanced by genetic code expansions, i.e. recoding, allowing the incorporation of the rare 21st and 22nd amino acids selenocysteine (Sec) and pyrrolysine (Pyl). We found Sec recoding in Jordarchaeia and all other Asgardarchaeota classes, which likely benefit from increased catalytic activities of Sec-containing enzymes. Pyl recoding on the other hand is restricted to Hodarchaeia in the Asgardarchaeota, making it the first reported non-methanogenic lineage with an inferred complete Pyl machinery, likely providing this class with an efficient mechanism for methylamine utilisation. Furthermore, we identified enzymes for the biosynthesis of ester-type lipids, characteristic of Bacteria and Eukaryotes, in both novel classes, supporting the hypothesis that mixed ether-ester lipids are a shared feature among Asgardarchaeota.

Predicting Lifestyle and Host From Positive Selection Data and Genome Properties in Oomycetes

Background: Host and niche shifts are a source of genomic and phenotypic diversi_cation as evidenced in parasitism. Most characteristic is core metabolism reduction as parasites adapt to a particular host, while the accessory genome often maintains a high degree of diversi_cation. However, selective pressures acting on the genome of such organisms are not fully understood. Results: Here, we developed a comparative genomic approach to study underlying adaptive trends in oomycetes, a eukaryotic phylum with a broad range of economically important plant and animal parasitic lifestyles. Our analysis reveals converging evolution on biological processes for oomycetes inhabiting similar niches. We _nd that certain functions, in particular carbohydrate metabolism, transport, and signaling, are important for host and environmental adaption in oomycetes. Discussion: Given the high correlation of lifestyle to genome properties in our oomycete dataset and the convergent evolution of fungal and oomycete genomes, we have developed a model that predicts plant pathogen lifestyles with high accuracy. Understanding how genomes and selective pressures correlate with lifestyle may be crucial to identify new emerging diseases and pandemic threats.

The Remarkable Metabolism of Vickermania ingenoplastis: Genomic Predictions

A recently redescribed two-flagellar trypanosomatid Vickermania ingenoplastis is insensitive to the classical inhibitors of respiration and thrives under anaerobic conditions. Using genomic and transcriptomic data, we analyzed its genes of the core metabolism and documented that subunits of the mitochondrial respiratory complexes III and IV are ablated, while those of complexes I, II, and V are all present, along with an alternative oxidase. This explains the previously reported conversion of glucose to acetate and succinate by aerobic fermentation. Glycolytic pyruvate is metabolized to acetate and ethanol by pyruvate dismutation, whereby a unique type of alcohol dehydrogenase (shared only with Phytomonas spp.) processes an excess of reducing equivalents formed under anaerobic conditions, leading to the formation of ethanol. Succinate (formed to maintain the glycosomal redox balance) is converted to propionate by a cyclic process involving three enzymes of the mitochondrial methyl-malonyl-CoA pathway, via a cyclic process, which results in the formation of additional ATP. The unusual structure of the V. ingenoplastis genome and its similarity with that of Phytomonas spp. imply their relatedness or convergent evolution. Nevertheless, a critical difference between these two trypanosomatids is that the former has significantly increased its genome size by gene duplications, while the latter streamlined its genome.

Predicting lifestyle and host from positive selection data and genome properties in oomycetes

BackgroundHost and niche shifts are a source of genomic and phenotypic diversification as evidenced in parasitism. Most characteristic is core metabolism reduction as parasites adapt to a particular host, while the accessory genome often maintains a high degree of diversification. However, selective pressures acting on the genome of such organisms are not fully understood.ResultsHere, we developed a comparative genomic approach to study underlying adaptive trends in oomycetes, a eukaryote phylum with a broad range of economically important plant and animal parasitic lifestyles. Our analysis reveals converging evolution on biological processes for oomycetes inhabiting similar niches. We find that certain functions, in particular carbohydrate metabolism, transport, and signaling, are important for host and environmental adaption in oomycetes.DiscussionGiven the high correlation of lifestyle to genome properties in our oomycete dataset and the convergent evolution of fungal and oomycete genomes, we have developed a model that predicts plant pathogen lifestyles with high accuracy. Understanding how genomes and selective pressures correlate with lifestyle may be crucial to identify new emerging diseases and pandemic threats.

Heterotrophic Euglenid Rhabdomonas Costata Resembles Its Phototrophic Relatives in Many Aspects of Molecular and Cell Biology

Euglenids represent a group of protists with diverse modes of feeding. To date, only a partial genomic sequence of Euglena gracilis and transcriptomes of several phototrophic and secondarily osmotrophic species are available, while primarily heterotrophic euglenids are seriously undersampled. In this work, we begin to fill this gap by presenting genomic and transcriptomic drafts of a primary osmotroph, Rhabdomonas costata. The current genomic assembly length of 100 Mbp is 14× smaller than that of E. gracilis. Despite being too fragmented for comprehensive gene prediction, comparison of the transcriptomic and genomic data revealed features of its introns, including several candidates for nonconventional introns. 16 % of transcripts bear a recognizable partial splice leader sequence. A set of 39,585 putative R. costata proteins were predicted from the transcriptome. Annotation of the mitochondrial core metabolism provides the first data on the facultatively anaerobic mitochondrion of R. costata, which in most respects resembles the mitochondrion of E. gracilis with certain level of streamlining. R. costata synthesises heme by a mitochondrial-cytoplasmatic C4 pathway with enzymes orthologous to those found in E. gracilis. The low percentage of green algae-affiliated genes, supports the ancestrally osmotrophic status of this species.