Amoebozoan testate amoebae illuminate the diversity of heterotrophs and the complexity of ecosystems throughout geological time.

Heterotrophic protists are vital in Earth's ecosystems, influencing carbon and nutrient cycles and occupying key positions in food webs as microbial predators. Fossils and molecular data suggest the emergence of predatory microeukaryotes and the transition to a eukaryote-rich marine environment by 800 million years ago (Ma). Neoproterozoic vase-shaped microfossils (VSMs) linked to Arcellinida testate amoebae represent the oldest evidence of heterotrophic microeukaryotes. This study explores the phylogenetic relationship and divergence times of modern Arcellinida and related taxa using a relaxed molecular clock approach. We estimate the origin of nodes leading to extant members of the Arcellinida Order to have happened during the latest Mesoproterozoic and Neoproterozoic (1054 to 661 Ma), while the divergence of extant infraorders postdates the Silurian. Our results demonstrate that at least one major heterotrophic eukaryote lineage originated during the Neoproterozoic. A putative radiation of eukaryotic groups (e.g., Arcellinida) during the early-Neoproterozoic sustained by favorable ecological and environmental conditions may have contributed to eukaryotic life endurance during the Cryogenian severe ice ages. Moreover, we infer that Arcellinida most likely already inhabited terrestrial habitats during the Neoproterozoic, coexisting with terrestrial Fungi and green algae, before land plant radiation. The most recent extant Arcellinida groups diverged during the Silurian Period, alongside other taxa within Fungi and flowering plants. These findings shed light on heterotrophic microeukaryotes' evolutionary history and ecological significance in Earth's ecosystems, using testate amoebae as a proxy.

Foraging mechanisms in excavate flagellates shed light on the functional ecology of early eukaryotes.

The phagotrophic flagellates described as "typical excavates" have been hypothesized to be morphologically similar to the Last Eukaryotic Common Ancestor and understanding the functional ecology of excavates may therefore help shed light on the ecology of these early eukaryotes. Typical excavates are characterized by a posterior flagellum equipped with a vane that beats in a ventral groove. Here, we combined flow visualization and observations of prey capture in representatives of the three clades of excavates with computational fluid dynamic modeling, to understand the functional significance of this cell architecture. We record substantial differences amongst species in the orientation of the vane and the beat plane of the posterior flagellum. Clearance rate magnitudes estimated from flow visualization and modeling are both like that of other similarly sized flagellates. The interaction between a vaned flagellum beating in a confinement is modeled to produce a very efficient feeding current at low energy costs, irrespective of the beat plane and vane orientation and of all other morphological variations. Given this predicted uniformity of function, we suggest that the foraging systems of typical excavates studied here may be good proxies to understand those potentially used by our distant ancestors more than 1 billion years ago.

The function of the feeding groove of 'typical excavate' flagellates.

Phagotrophic flagellates are the main consumers of bacteria and picophytoplankton. Despite their ecological significance in the 'microbial loop', many of their predation mechanisms remain unclear. 'Typical excavates' bear a ventral groove, where prey is captured for ingestion. The consequences of feeding through a 'semi-rigid' furrow on the prey size range have not been explored. An unidentified moving element called 'the wave' that sweeps along the bottom of the groove toward the site of phagocytosis has been observed in a few species; its function is unclear. We investigated the presence, behavior, and function of the wave in four species from the three excavate clades (Discoba, Metamonada, and Malawimonadida) and found it present in all studied cases, suggesting the potential homology of this feature across all three groups. The wave displayed a species-specific behavior and was crucial for phagocytosis. The morphology of the feeding groove had an upper-prey size limit for successful prey captures, but smaller particles were not constrained. Additionally, the ingestion efficiencies were species dependent. By jointly studying these feeding traits, we speculate on adaptations to differences in food availability to better understand their ecological functions.

ATAD3 Proteins: Unique Mitochondrial Proteins Essential for Life in Diverse Eukaryotic Lineages.

ATAD3 proteins (ATPase family AAA domain-containing protein 3) are unique mitochondrial proteins that arose deep in the eukaryotic lineage but that are surprisingly absent from the Fungi and Amoebozoa. These ~600 amino acid proteins are anchored in the inner mitochondrial membrane and are essential in metazoans and Arabidopsis thaliana. ATAD3s comprise a C-terminal AAA+ matrix domain and an ATAD3_N domain that is located primarily in the inner membrane space but potentially extends into cytosol to interact with the ER. Sequence and structural alignments indicate ATAD3 proteins are most similar to classic chaperone unfoldases in AAA+ family, suggesting that they operate in mitochondrial protein quality control. A. thaliana has four ATAD3 genes in two distinct clades that appear first in the seed plants, and both clades are essential for viability. The four genes are generally coordinately expressed, and transcripts are highest in growing apices and imbibed seeds. Plants with disrupted ATAD3 have reduced growth, aberrant mitochondrial morphology, diffuse nucleoids and reduced oxidative phosphorylation complex I. These and other pleiotropic phenotypes are also observed in ATAD3 mutants in metazoans. Here we discuss the distribution of ATAD3 proteins as they have evolved in the plant kingdom, their unique structure, what we know about their function in plants, and the challenges in determining their essential roles in mitochondria.

Restriction of intraflagellar transport to some microtubule doublets: An opportunity for cilia diversification?

Cilia are unique eukaryotic organelles and exhibit remarkable conservation across evolution. Nevertheless, very different types of configurations are encountered, raising the question of their evolution. Cilia are constructed by intraflagellar transport (IFT), the movement of large protein complexes or trains that deliver cilia components to the distal tip for assembly. Recent data revealed that IFT trains are restricted to some but not all nine doublet microtubules in the protist Trypanosoma brucei. Here, we propose that restricted positioning of IFT trains could offer potent options for cilia to evolve towards more complex (addition of new structural elements like in spermatozoa) or simpler configuration (loss of some elements like in primary cilia), and therefore be a driver of cilia diversification. We present two hypotheses to explain how IFT trains could be restricted to some doublets, either by a triage process taking place at the basal body level or by the development of molecular differences between ciliary microtubules.

Evolutionary Adjustment of tRNA Identity Rules in Bacillariophyta for Recognition by an Aminoacyl-tRNA Synthetase Adds a Facet to the Origin of Diatoms.

Error-free protein synthesis relies on the precise recognition by the aminoacyl-tRNA synthetases of their cognate tRNAs in order to attach the corresponding amino acid. A concept of universal tRNA identity elements requires the aminoacyl-tRNA synthetases provided by the genome of an organism to match the identity elements found in the cognate tRNAs in an evolution-independent manner. Identity elements tend to cluster in the tRNA anticodon and acceptor stem regions. However, in the arginine system, in addition to the anticodon, the importance of nucleotide A20 in the tRNA D-loop for cognate enzyme recognition has been a sustained feature for arginyl-tRNA synthetase in archaea, bacteria and in the nuclear-encoded cytosolic form in mammals and plants. However, nuclear-encoded mitochondrial arginyl-tRNA synthetase, which can be distinguished from its cytosolic form by the presence or absence of signature motifs, dispenses with the A20 requirement. An examination of several hundred non-metazoan organisms and their corresponding tRNAArg substrates has confirmed this general concept to a large extent and over numerous phyla. However, some Stramenopiles, and in particular, Diatoms (Bacillariophyta) present a notable exception. Unusually for non-fungal organisms, the nuclear genome encodes tRNAArg isoacceptors with C or U at position 20. In this case one of two nuclear-encoded cytosolic arginyl-tRNA synthetases has evolved to become insensitive to the nature of the D-loop identity element. The other, with a binding pocket that is compatible with tRNAArg-A20 recognition, is targeted to organelles that encode solely such tRNAs.

Phylogenetic reconstruction and evolution of the Rab GTPase gene family in Amoebozoa.

Rab GTPase is a paralog-rich gene family that controls the maintenance of the eukaryotic cell compartmentalization system. Diverse eukaryotes have varying numbers of Rab paralogs. Currently, little is known about the evolutionary pattern of Rab GTPase in most major eukaryotic 'supergroups'. Here, we present a comprehensive phylogenetic reconstruction of the Rab GTPase gene family in the eukaryotic 'supergroup' Amoebozoa, a diverse lineage represented by unicellular and multicellular organisms. We demonstrate that Amoebozoa conserved 20 of the 23 ancestral Rab GTPases predicted to be present in the last eukaryotic common ancestor and massively expanded several 'novel' in-paralogs. Due to these 'novel' in-paralogs, the Rab family composition dramatically varies between the members of Amoebozoa; as a consequence, 'supergroup'-based studies may significantly change our current understanding of the evolution and diversity of this gene family. The high diversity of the Rab GTPase gene family in Amoebozoa makes this 'supergroup' a key lineage to study and advance our knowledge of the evolution of Rab in Eukaryotes.

Decontamination, pooling and dereplication of the 678 samples of the Marine Microbial Eukaryote Transcriptome Sequencing Project.

OBJECTIVES: Complex algae are photosynthetic organisms resulting from eukaryote-to-eukaryote endosymbiotic-like interactions. Yet the specific lineages and mechanisms are still under debate. That is why large scale phylogenomic studies are needed. Whereas available proteomes provide a limited diversity of complex algae, MMETSP (Marine Microbial Eukaryote Transcriptome Sequencing Project) transcriptomes represent a valuable resource for phylogenomic analyses, owing to their broad and rich taxonomic sampling, especially of photosynthetic species. Unfortunately, this sampling is unbalanced and sometimes highly redundant. Moreover, we observed contaminated sequences in some samples. In such a context, tree inference and readability are impaired. Consequently, the aim of the data processing reported here is to release a unique set of clean and non-redundant transcriptomes produced through an original protocol featuring decontamination, pooling and dereplication steps. DATA DESCRIPTION: We submitted 678 MMETSP re-assembly samples to our parallel consolidation pipeline. Hence, we combined 423 samples into 110 consolidated transcriptomes, after the systematic removal of the most contaminated samples (186). This approach resulted in a total of 224 high-quality transcriptomes, easy to use and suitable to compute less contaminated, less redundant and more balanced phylogenies.

Origin and Early Evolution of the Eukaryotic Cell.

The origin of eukaryotes has been defined as the major evolutionary transition since the origin of life itself. Most hallmark traits of eukaryotes, such as their intricate intracellular organization, can be traced back to a putative common ancestor that predated the broad diversity of extant eukaryotes. However, little is known about the nature and relative order of events that occurred in the path from preexisting prokaryotes to this already sophisticated ancestor. The origin of mitochondria from the endosymbiosis of an alphaproteobacterium is one of the few robustly established events to which most hypotheses on the origin of eukaryotes are anchored, but the debate is still open regarding the time of this acquisition, the nature of the host, and the ecological and metabolic interactions between the symbiotic partners. After the acquisition of mitochondria, eukaryotes underwent a fast radiation into several major clades whose phylogenetic relationships have been largely elusive. Recent progress in the comparative analyses of a growing number of genomes is shedding light on the early events of eukaryotic evolution as well as on the root and branching patterns of the tree of eukaryotes. Here I discuss current knowledge and debates on the origin and early evolution of eukaryotes. I focus particularly on how phylogenomic analyses have challenged some of the early assumptions about eukaryotic evolution, including the widespread idea that mitochondrial symbiosis in an archaeal host was the earliest event in eukaryogenesis.

Broadly sampled orthologous groups of eukaryotic proteins for the phylogenetic study of plastid-bearing lineages.

OBJECTIVES: Identifying orthology relationships among sequences is essential to understand evolution, diversity of life and ancestry among organisms. To build alignments of orthologous sequences, phylogenomic pipelines often start with all-vs-all similarity searches, followed by a clustering step. For the protein clusters (orthogroups) to be as accurate as possible, proteomes of good quality are needed. Here, our objective is to assemble a data set especially suited for the phylogenomic study of algae and formerly photosynthetic eukaryotes, which implies the proper integration of organellar data, to enable distinguishing between several copies of one gene (paralogs), taking into account their cellular compartment, if necessary. DATA DESCRIPTION: We submitted 73 top-quality and taxonomically diverse proteomes to OrthoFinder. We obtained 47,266 orthogroups and identified 11,775 orthogroups with at least two algae. Whenever possible, sequences were functionally annotated with eggNOG and tagged after their genomic and target compartment(s). Then we aligned and computed phylogenetic trees for the orthogroups with IQ-TREE. Finally, these trees were further processed by identifying and pruning the subtrees exclusively composed of plastid-bearing organisms to yield a set of 31,784 clans suitable for studying photosynthetic organism genome evolution.

Friend turned foe: A curious case of disrupted endosymbiotic homeostasis promoting the Warburg effect in sepsis.

Sepsis is a grievous health concern with limited understanding of its precise etiology. Although studies on sepsis have implicated the Warburg effect (mitigation of mitochondrial oxidative phosphorylation, as evident from aerobic glycolysis), we propose that an evolutionary perspective might further unravel its etiology. The endosymbiotic theory suggests that evolution of a eukaryotic cell is a consequence of the fruitful association between an archaea (Asgard) and an alphaproteobacterium (Rickettsia). We hypothesize that, during pathological conditions like sepsis, such endosymbiotic homeostasis between the two systems is perturbed. We underscore the fact (supported by in silico homology analyses) that during sepsis, the Asgard component of a cell is promoted to trigger aerobic glycolysis as well as the innate immune response (spearheaded by the TLR pathway), while suppressing the Rickettsia counterpart, thereby promoting the Warburg effect. It might be this discord between the two endosymbiotic partners (Asgard and Rickettsia-derived cellular components) that promotes sepsis.

Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes.

The conservation of orthologs of most subunits of the origin recognition complex (ORC) has served to propose that the whole complex is common to all eukaryotes. However, various uncertainties have arisen concerning ORC subunit composition in a variety of lineages. Also, it is unclear whether the ancestral diversification of ORC in eukaryotes was accompanied by the neofunctionalization of some subunits, for example, role of ORC1 in centriole homeostasis. We have addressed these questions by reconstructing the distribution and evolutionary history of ORC1-5/CDC6 in a taxon-rich eukaryotic data set. First, we identified ORC subunits previously undetected in divergent lineages, which allowed us to propose a series of parsimonious scenarios for the origin of this multiprotein complex. Contrary to previous expectations, we found a global tendency in eukaryotes to increase or decrease the number of subunits as a consequence of genome duplications or streamlining, respectively. Interestingly, parasites show significantly lower number of subunits than free-living eukaryotes, especially those with the lowest genome size and gene content metrics. We also investigated the evolutionary origin of the ORC1 role in centriole homeostasis mediated by the PACT region in human cells. In particular, we tested the consequences of reducing ORC1 levels in the centriole-containing green alga Chlamydomonas reinhardtii. We found that the proportion of centrioles to flagella and nuclei was not dramatically affected. This, together with the PACT region not being significantly more conserved in centriole-bearing eukaryotes, supports the notion that this neofunctionalization of ORC1 would be a recent acquisition rather than an ancestral eukaryotic feature.

An Integrated Model of Minor Intron Emergence and Conservation.

Minor introns constitute <0.5% of the introns in the human genome and have remained an enigma since their discovery. These introns are removed by a distinct splicing complex, the minor spliceosome. Both are ancient, tracing back to the last eukaryotic common ancestor (LECA), which is reflected by minor intron enrichment in specific gene families, such as the mitogen activated-protein kinase kinases, voltage-gated sodium and calcium ion channels, and E2F transcription factors. Most minor introns occur as single introns in genes with predominantly major introns. Due to this organization, minor intron-containing gene (MIG) expression requires the coordinated action of two spliceosomes, which increases the probability of missplicing. Thus, one would expect loss of minor introns via purifying selection. This has resulted in complete minor intron loss in at least nine eukaryotic lineages. However, minor introns are highly conserved in land plants and metazoans, where their importance is underscored by embryonic lethality when the minor spliceosome is inactivated. Conditional inactivation of the minor spliceosome has shown that rapidly dividing progenitor cells are highly sensitive to minor spliceosome loss. Indeed, we found that MIGs were significantly enriched in a screen for genes essential for survival in 341 cycling cell lines. Here, we propose that minor introns inserted randomly into genes in LECA or earlier and were subsequently conserved in genes crucial for cycling cell survival. We hypothesize that the essentiality of MIGs allowed minor introns to endure through the unicellularity of early eukaryotic evolution. Moreover, we identified 59 MIGs that emerged after LECA, and that many of these are essential for cycling cell survival, reinforcing our essentiality model for MIG conservation. This suggests that minor intron emergence is dynamic across eukaryotic evolution, and that minor introns should not be viewed as molecular fossils. We also posit that minor intron splicing was co-opted in multicellular evolution as a regulatory switch for en masse control of MIG expression and the biological processes they regulate. Specifically, this mode of regulation could control cell proliferation and thus body size, an idea supported by domestication syndrome, wherein MIGs are enriched in common candidate animal domestication genes.

Characterization of Nme5-Like Gene/Protein from the Red Alga Chondrus Crispus.

The Nme gene/protein family of nucleoside diphosphate kinases (NDPK) was originally named after its member Nm23-H1/Nme1, the first identified metastasis suppressor. Human Nme proteins are divided in two groups. They all possess nucleoside diphosphate kinase domain (NDK). Group I (Nme1-Nme4) display a single type NDK domain, whereas Group II (Nme5-Nme9) display a single or several different NDK domains, associated or not associated with extra-domains. Data strongly suggest that, unlike Group I, none of the members of Group II display measurable NDPK activity, although some of them autophosphorylate. The multimeric form is required for the NDPK activity. Group I proteins are known to multimerize, while there are no data on the multimerization of Group II proteins. The Group II ancestral type protein was shown to be conserved in several species from three eukaryotic supergroups. Here, we analysed the Nme protein from an early branching eukaryotic lineage, the red alga Chondrus crispus. We show that the ancestral type protein, unlike its human homologue, was fully functional multimeric NDPK with high affinity to various types of DNA and dispersed localization throughout the eukaryotic cell. Its overexpression inhibits both cell proliferation and the anchorage-independent growth of cells in soft agar but fails to deregulate cell apoptosis. We conclude that the ancestral gene has changed during eukaryotic evolution, possibly in correlation with the protein function.

On the Origin of Iron/Sulfur Cluster Biosynthesis in Eukaryotes.

Iron and sulfur are indispensable elements of every living cell, but on their own these elements are toxic and require dedicated machineries for the formation of iron/sulfur (Fe/S) clusters. In eukaryotes, proteins requiring Fe/S clusters (Fe/S proteins) are found in or associated with various organelles including the mitochondrion, endoplasmic reticulum, cytosol, and the nucleus. These proteins are involved in several pathways indispensable for the viability of each living cell including DNA maintenance, protein translation and metabolic pathways. Thus, the formation of Fe/S clusters and their delivery to these proteins has a fundamental role in the functions and the evolution of the eukaryotic cell. Currently, most eukaryotes harbor two (located in cytosol and mitochondrion) or three (located in plastid) machineries for the assembly of Fe/S clusters, but certain anaerobic microbial eukaryotes contain sulfur mobilization (SUF) machineries that were previously thought to be present only in archaeal linages. These machineries could not only stipulate which pathway was present in the last eukaryotic common ancestor (LECA), but they could also provide clues regarding presence of an Fe/S cluster machinery in the proto-eukaryote and evolution of Fe/S cluster assembly machineries in all eukaryotes.

Metagenomes from Coastal Marine Sediments Give Insights into the Ecological Role and Cellular Features of Loki- and Thorarchaeota.

The genomes of Asgard Archaea, a novel archaeal proposed superphylum, share an enriched repertoire of eukaryotic signature genes and thus promise to provide insights into early eukaryote evolution. However, the distribution, metabolisms, cellular structures, and ecology of the members within this superphylum are not well understood. Here we provide a meta-analysis of the environmental distribution of the Asgard archaea, based on available 16S rRNA gene sequences. Metagenome sequencing of samples from a salt-crusted lagoon on the Baja California Peninsula of Mexico allowed the assembly of a new Thorarchaeota and three Lokiarchaeota genomes. Comparative analyses of all known Lokiarchaeota and Thorarchaeota genomes revealed overlapping genome content, including central carbon metabolism. Members of both groups contained putative reductive dehalogenase genes, suggesting that these organisms might be able to metabolize halogenated organic compounds. Unlike the first report on Lokiarchaeota, we identified genes encoding glycerol-1-phosphate dehydrogenase in all Loki- and Thorarchaeota genomes, suggesting that these organisms are able to synthesize bona fide archaeal lipids with their characteristic glycerol stereochemistry.IMPORTANCE Microorganisms of the superphylum Asgard Archaea are considered to be the closest living prokaryotic relatives of eukaryotes (including plants and animals) and thus promise to give insights into the early evolution of more complex life forms. However, very little is known about their biology as none of the organisms has yet been cultivated in the laboratory. Here we report on the ecological distribution of Asgard Archaea and on four newly sequenced genomes of the Lokiarchaeota and Thorarchaeota lineages that give insight into possible metabolic features that might eventually help to identify these enigmatic groups of archaea in the environment and to culture them.

Oxygenated Mesoproterozoic lake revealed through magnetic mineralogy.

Terrestrial environments have been suggested as an oxic haven for eukaryotic life and diversification during portions of the Proterozoic Eon when the ocean was dominantly anoxic. However, iron speciation and Fe/Al data from the ca. 1.1-billion-year-old Nonesuch Formation, deposited in a large lake and bearing a diverse assemblage of early eukaryotes, are interpreted to indicate persistently anoxic conditions. To shed light on these distinct hypotheses, we analyzed two drill cores spanning the transgression into the lake and its subsequent shallowing. While the proportion of highly reactive to total iron (FeHR/FeT) is consistent through the sediments and typically in the range taken to be equivocal between anoxic and oxic conditions, magnetic experiments and petrographic data reveal that iron exists in three distinct mineral assemblages resulting from an oxycline. In the deepest waters, reductive dissolution of iron oxides records an anoxic environment. However, the remainder of the sedimentary succession has iron oxide assemblages indicative of an oxygenated environment. At intermediate water depths, a mixed-phase facies with hematite and magnetite indicates low oxygen conditions. In the shallowest waters of the lake, nearly every iron oxide has been oxidized to its most oxidized form, hematite. Combining magnetics and textural analyses results in a more nuanced understanding of ambiguous geochemical signals and indicates that for much of its temporal duration, and throughout much of its water column, there was oxygen in the waters of Paleolake Nonesuch.

Relative timing of mitochondrial endosymbiosis and the "pre-mitochondrial symbioses" hypothesis.

The origin of eukaryotes stands as a major open question in biology. Central to this question is the nature and timing of the origin of the mitochondrion, an ubiquitous eukaryotic organelle originated by the endosymbiosis of an alphaproteobacterial ancestor. Different hypotheses disagree, among other aspects, on whether mitochondria were acquired early or late during eukaryogenesis. Similarly, the nature and complexity of the receiving host is debated, with models ranging from a simple prokaryotic host to an already complex proto-eukaryote. Here, I will discuss recent findings from phylogenomics analyses of extant genomes that are shedding light into the evolutionary origins of the eukaryotic ancestor, and which suggest a later acquisition of alpha-proteobacterial derived proteins as compared to those with different bacterial ancestries. I argue that simple eukaryogenesis models that assume a binary symbiosis between an archaeon host and an alpha-proteobacterial proto-mitochondrion cannot explain the complex chimeric nature that is inferred for the eukaryotic ancestor. To reconcile existing hypotheses with the new data, I propose the "pre-mitochondrial symbioses" hypothesis that provides a framework for eukaryogenesis scenarios involving alternative symbiotic interactions that predate the acquisition of mitochondria. © 2018 The Authors. IUBMB Life published by Wiley Periodicals, Inc. on behalf of International Union of Biochemistry and Molecular Biology, 70(12):1188-1196, 2018.

A Novel Eukaryotic Denitrification Pathway in Foraminifera.

Benthic foraminifera are unicellular eukaryotes inhabiting sediments of aquatic environments. Several species were shown to store and use nitrate for complete denitrification, a unique energy metabolism among eukaryotes. The population of benthic foraminifera reaches high densities in oxygen-depleted marine habitats, where they play a key role in the marine nitrogen cycle. However, the mechanisms of denitrification in foraminifera are still unknown, and the possibility of a contribution of associated bacteria is debated. Here, we present evidence for a novel eukaryotic denitrification pathway that is encoded in foraminiferal genomes. Large-scale genome and transcriptomes analyses reveal the presence of a denitrification pathway in foraminifera species of the genus Globobulimina. This includes the enzymes nitrite reductase (NirK) and nitric oxide reductase (Nor) as well as a wide range of nitrate transporters (Nrt). A phylogenetic reconstruction of the enzymes' evolutionary history uncovers evidence for an ancient acquisition of the foraminiferal denitrification pathway from prokaryotes. We propose a model for denitrification in foraminifera, where a common electron transport chain is used for anaerobic and aerobic respiration. The evolution of hybrid respiration in foraminifera likely contributed to their ecological success, which is well documented in palaeontological records since the Cambrian period.

Horizontal Gene Transfer From Bacteria and Plants to the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis.

Arbuscular mycorrhizal fungi (AMF) belong to Glomeromycotina, and are mutualistic symbionts of many land plants. Associated bacteria accompany AMF during their lifecycle to establish a robust tripartite association consisting of fungi, plants and bacteria. Physical association among this trinity provides possibilities for the exchange of genetic materials. However, very few horizontal gene transfer (HGT) from bacteria or plants to AMF has been reported yet. In this study, we complement existing algorithms by developing a new pipeline, Blast2hgt, to efficiently screen for putative horizontally derived genes from a whole genome. Genome analyses of the glomeromycete Rhizophagus irregularis identified 19 fungal genes that had been transferred between fungi and bacteria/plants, of which seven were obtained from bacteria. Another 18 R. irregularis genes were found to be recently acquired from either plants or bacteria. In the R. irregularis genome, gene duplication has contributed to the expansion of three foreign genes. Importantly, more than half of the R. irregularis foreign genes were expressed in various transcriptomic experiments, suggesting that these genes are functional in R. irregularis. Functional annotation and available evidence showed that these acquired genes may participate in diverse but fundamental biological processes such as regulation of gene expression, mitosis and signal transduction. Our study suggests that horizontal gene influx through endosymbiosis is a source of new functions for R. irregularis, and HGT might have played a role in the evolution and symbiotic adaptation of this arbuscular mycorrhizal fungus.