Biology subjects

Kamikawa, R.

Publications and source records attributed to Kamikawa, R..

17 recordsLinked to original sources

bioRxiv2026

Inverse relationship between mitochondrial and non-coding nuclear DNA content in free-living kinetoplastids

The evolution of genome size and eukaryotic genome organisation has puzzled evolutionary biologists for decades. Are differences in DNA content and protein-coding capacity of eukaryotic genomes a result of natural selection, or neutral processes? If they were shaped by natural selection, which features might be connected with these differences: cell volume, ecological strategy, availability of nutrients, etc.? Kinetoplastids are protists with compact nuclear genomes that almost entirely lack introns, but whose mitochondrial DNA content (kDNA) can rival that of their nuclei. We hypothesised that the reduction in non-protein coding nuclear DNA content during the evolution of kinetoplastids is connected with an increase in kDNA content: species with larger fractions of total cellular DNA that is allocated to kDNA will have concomitantly smaller fractions of non-coding DNA in the nuclear genome. We developed a framework for estimation of DNA content in both the mitochondria and nuclei from quantitative fluorescence microscopy data, and inferred the fraction of non-coding DNA in nuclear genomes based on the combination of transcriptomic and fluorescence imaging data. Across 10 genetically distant isolates from diverse free-living kinetoplastid lineages, there is indeed a trend towards a lower proportion of non-protein-coding nuclear DNA when kDNA proportion is higher relative to the total DNA in the cell. This observation is consistent with the hypothesis that in free-living kinetoplastids, mitochondrial and nuclear genomes might co-evolve in terms of their DNA content. This finding raises the possibility that natural selection acts on genome size evolution in kinetoplastids, and contributes evidence and methodology to address this question more broadly in eukaryotes.

evolutionary biology↗

bioRxiv2026

Ecological Role of the Heterotrophic Protist Aurantiochytrium (Labyrinthulomycetes) as a Key Consumer of Viral-Induced Dissolved Organic Matter Following the Lysis of the Red Tide-forming Microalga Heterosigma akashiwo

Marine algal blooms play a vital role in oceanic carbon cycling, yet the ecological consequences of algal organic matter released following their collapse via viral infection are poorly understood. Recent studies have shown that viral infection dramatically alters the hosts intracellular metabolite composition, and the subsequent viral lysate selectively promotes the growth of specific prokaryotic populations. This study aimed to elucidate the effect of organic matter derived from healthy and virus-infected cells of the bloom-forming alga Heterosigma akashiwo on the growth of heterotrophic eukaryotes, specifically Labyrinthulomycetes. These marine protists are primarily saprotrophic or predatory and contribute to dissolved organic matter (DOM) decomposition and nutrient cycling. Our field monitoring in Osaka Bay over 12 months revealed that while the overall Labyrinthulomycetes community showed no clear seasonality, specific populations of the protists co-occurred with Heterosigma akashiwo. To mechanistically investigate the potential trophic linkage suggested by these field observations, a co-culture system comprising H. akashiwo, its specific virus (HaV53), and Aurantiochytrium sp. NBRC102614, used here as a model Labyrinthulomycete, was established. In the co-culture experiments, viral lysis of H. akashiwo led to a significant increase in the cell density of Aurantiochytrium sp., demonstrating that Aurantiochytrium can thrive on substrates derived from the virus-infected alga, such as viral-induced dissolved organic matter (vDOM). These findings highlight that heterotrophic Labyrinthulomycetes are one of key consumers of virus-modified organic matter, playing a pivotal role in carbon cycling following the collapse of harmful algal blooms and influencing carbon transfer in coastal microbial food webs. IMPORTANCEMarine ecosystems are tightly regulated by the interplay between microalgae, viruses, and heterotrophic eukaryotes, yet their roles within this network have long been underestimated. Accordingly, this study aimed to provide an overview of the dynamics of environmental microalgae and heterotrophic eukaryotes, namely Heterosigma species and Labyrinthulomycetes, and to elucidate the impact of virus-infected Heterosigma akashiwo on the growth and proliferation of Aurantiochytrium species within heterotrophic Labyrinthulomycetes. This study revealed the dynamics of several Labyrinthulomycetes species associated with Heterosigma populations in coastal marine environments and demonstrated that Aurantiochytrium species have the capacity to redistribute carbon, such as by utilizing vDOM released during the termination of Heterosigma blooms via viral infection, thereby repositioning Aurantiochytrium from a passive component of Heterosigma viral infection toward an active ecological agent that facilitates energy transfer and contributes to the maintenance of microalgal community dynamics. Overall, this work provides new insights into the fate of virus-infected Heterosigma in coastal marine systems mediated by heterotrophic Labyrinthulomycetes, particularly Aurantiochytrium species, thereby filling an important knowledge gap in microbial ecology.

microbiology↗

bioRxiv2025

Carbon monoxide-driven proton respiration enables facultative anaerobes to survive electron acceptor limitation

Diverse microorganisms couple the oxidation of carbon monoxide gas (CO) to the reduction of protons, producing hydrogen gas (H2). This energy-conserving process is mediated by the nickel-containing CO dehydrogenase/energy-converting hydrogenase (Ni-CODH/ECH). Yielding only a small supply of energy, the physiological role of this process at environmentally relevant CO levels remains unresolved. Here, we show that Ni-CODH/ECH enables metabolically flexible facultative anaerobes within the Anoxybacillaceae to survive electron acceptor limitation. Analysis of 387 Anoxybacillaceae genomes revealed that Ni-CODH/ECH had a patchy distribution and, with one exception, was mutually exclusive with the aerobic molybdenum-containing CODH. Culture experiments using the three isolates (Parageobacillus sp. G301, P. thermoglucosidasius NBRC 107763, and Thermolongibacillus altinsuensis B1-1) demonstrated that CO-dependent proton respiration is activated during stationary phase when exogenous electron acceptors are limiting, enhancing cell density 1.2-to 1.5-fold under 25% CO, whereas no effect was observed in a Ni-CODH knockout ({Delta}cooCSF) strain. RNA-seq analysis of strain G301 under twelve conditions revealed that Ni-CODH genes reached 2,000-12,500 TPM (top 0.2-1.9% of all genes) during stationary phase, independent of CO presence, under the predicted control of the redox-dependent transcriptional repressor Rex. {Delta}cooCSF cultures accumulated more trace CO than the wild-type, suggesting trace CO uptake by the wild-type. Thus, Ni-CODH/ECH is a redox-regulated auxiliary energy-conservation system that supports adaptation to electron acceptor limitation. Given the continual environmental supply of the two substrates for this enzyme, we propose CO-dependent proton respiration is a dependable way for metabolically flexible microorganisms to stay energized in spatiotemporally variable environments. Significance statementMicroorganisms are frequently challenged to survive in environments where both energy sources and electron acceptors are limited. We reveal that facultative anaerobes activate a respiratory process that utilizes carbon monoxide (CO) and protons to survive under electron acceptor limitation. This hydrogenogenic CO-oxidizing reaction, termed CO-dependent proton respiration, is catalyzed by an ancient and minimal complex, the nickel-containing CO dehydrogenase/energy-converting hydrogenase. Although the reaction yields barely enough energy to translocate protons, this complex provides a reliable lifeline by extracting energy from trace CO and protons that are ubiquitous in nature, even when other electron acceptors are depleted. The widespread distribution of this complex across bacteria and archaea suggests that it provides a universal adaptive advantage for life under energy-limited conditions.

microbiology↗

bioRxiv2025

Impact of acetate on CO2 fixation pathways in thermophilic and hydrogenotrophic bacteria

The Wood-Ljungdahl (WL) pathway and reductive tricarboxylic acid (rTCA) cycle are the dominant chemolithotrophic CO2 fixation pathways in bacteria inhabiting aphotic geothermal and deep-sea hydrothermal ecosystems. However, the activity of these bacterial metabolic systems in ecosystems with available organic carbons remains unclear. Here, we examined the impact of extracellular acetate on the CO2-fixation pathways of three thermophilic hydrogen-oxidizing and non-acetogenic bacteria using 13C tracer-based metabolomics. Under chemolithoautotrophic conditions, Thermodesulfatator indicus and Hydrogenobacter thermophilus fixed CO2 through the WL pathway and rTCA cycle, respectively, whereas Thermovibrio ammonificans, which has been suggested to operate both of these pathways, exhibited significant CO2 fixation through only the rTCA cycle. Under chemolithomixotrophic conditions with acetate, H. thermophilus and T. ammonificans assimilated both CO2 and acetate via the rTCA cycle. In contrast, acetate suppressed CO2 fixation through the WL pathway in T. indicus and was used as the primary carbon source under chemolithomixotrophic conditions. These results suggest that the contribution of the WL pathway for CO2 fixation might be overestimated in ecosystems where acetate is available. Moreover, the present findings indicate that simultaneous CO2 fixation through both the WL pathway and rTCA cycle in a cell, which has been proposed as a possible metabolic strategy for CO2-fixation in ancestral life, is not advantageous in extant microorganisms.

microbiology↗

bioRxiv2025

Positive selection of a starch synthesis gene and phenotypic differentiation of starch accumulation in symbiotic and free-living coral symbiont dinoflagellate species

Symbiosis is a basis for species diversification through interactions between organisms. In tropical and subtropical oceans, dinoflagellate symbionts belonging to the family Symbiodiniaceae, including the genus Symbiodinium, support the flourishment of cnidarian hosts, including corals, and thereby the ecology of oligotrophic oceans through their photosynthate carbon transfers. Although the genus Symbiodinium includes both free-living and symbiotic species, the detailed genetic background of their lifestyle differences remains unclear. In this study, we identified candidate genes involved in the evolutionary acquisition or maintenance of symbiosis in Symbiodinium spp. by detecting genes that have undergone positive selection during symbiotic and free-living lifestyle diversification. Using multiple Symbiodinium genomes to detect positive selection, 35 genes were identified, including a gene encoding soluble starch synthase SSY1 and genes related to metabolite secretion, which may be preferred for symbiotic lifestyles. In particular, our in silico analyses revealed that the SSY1 gene family has undergone extensive gene duplications in an ancestral dinoflagellate, and that the mutations detected as positive selection have occurred in the intrinsically disordered region of one of the homologs. Consistent with molecular evolution, the phenotypes of intracellular starch synthesis/accumulation were distinct between the symbiotic and free-living species of Symbiodinium when cultured under different pH and nitrogen conditions. These results provide molecular and phenotypic insights into symbiotic Symbiodinium-coral relationships. Significance statementClarifying how coral symbiont algae of the family Symbiodiniaceae are functionally diversified is crucial for understanding the molecular mechanisms of symbiotic relationships and interactions in animal-algal symbioses. However, gene-level molecular evolution that contributes to symbiotic relationships remains unclear. Our genome-wide single-gene analyses of the genus Symbiodinium, comprising both symbiotic and free-living species, successfully detected several dozen protein-coding genes that underwent symbiont-specific positive selection after divergence from the free-living species in the genus. Furthermore, our cultivation experiments demonstrated differences in photosynthate-related phenotypes between the symbiotic and free-living species. Our findings provide a key to illuminating the molecular evolution involved in phenotypic changes that potentially contribute to symbiotic lifestyles in Symbiodinium.

evolutionary biology↗

bioRxiv2025

Complete mitochondrial genomes of ancyromonads provide clues for the gene content and genome structures of ancestral mitochondria.

Mitochondria of eukaryotic cells are direct descendants of an endosymbiotic bacterium related to Alphaproteobacteria. These organelles retain their own genomes, which are highly reduced and divergent when compared to those of their bacterial relatives. To better understand the trajectory of mitochondrial genome evolution from the last eukaryotic common ancestor (LECA) to extant species, mitochondrial genome sequences from phylogenetically diverse lineages of eukaryotes - particularly protists - are essential. For this reason, we focused on the mitochondrial genomes of Ancyromonadida, an independent and understudied protist lineage in the eukaryote tree of life. Here we report the mitochondrial genomes from three Ancyromonadida: Ancyromonas sigmoides, Nutomonas longa, and Fabomonas tropica. Our analyses reveal that these mitochondrial genomes are circularly mapping molecules that feature protein-coding inverted repeats. This inverted repeat structure has been observed in other mitochondrial genomes but is patchily distributed over the tree of eukaryotes. Ancyromonad mitochondrial genomes possess several protein-coding genes which have not been detected from any other mitochondrial genomes of eukaryotes sequenced to date, thereby extending the known mitochondrial gene repertoire of ancestral eukaryotes, including LECA. These findings significantly expand our understanding of mitochondrial genome diversity across eukaryotes, shedding light on the early phases of mitochondrial genome evolution in eukaryotes.

evolutionary biology↗

bioRxiv2024

Viral infection to the raphidophycean alga Heterosigma akashiwo affects both intracellular organic matter composition and dynamics of a coastal prokaryotic community

Marine microalgae play a crucial role in marine ecosystem by supplying dissolved organic matter to heterotrophic prokaryotes, which mediate the microbial loop. Microalgae are often infected by viruses, and in infected cells (virocells), the viruses modulate and often change the host metabolism for propagation and thereby endo-metabolites. However, the impact of algal virocells on prokaryotic communities is not fully been understood. In this study, we investigated whether lysates from virocell of Heterosigma akashiwo, a globally prevalent bloom-forming raphidophycean alga, causes shifts inn prokaryotic community structure, and which metabolic compounds in the viral lysate might affect the surrounding prokaryotic populations. Using microcosm experiments, we cultured prokaryotic communities with a dissolved fraction derived from the viral lysate (VDF) of H. akashiwo. Results revealed that certain prokaryotic populations assigned as the Vibrio spp. pathogenic against fish and crustaceans grew specifically responding to the VDF. These Vibrio species possessed a gene module for branched-chain amino acids transporters, which were revealed to be enriched in VDF by gas chromatography-mass spectrometry analysis. Altogether, our findings suggest that viral infection-induced changes in biochemical properties of H. akashiwo cells can promote the growth of taxonomically and metabolically different prokaryotic populations, potentially impacting higher trophic-level consumers in marine ecosystems. HighlightsO_LIThe effect of viral infection to microalgae on marine prokaryotes was investigated. C_LIO_LIViral lysate of Heterosigma akashiwo promoted growth of certain Vibrio population. C_LIO_LIThose Vibrio likely have ability to utilize the compounds enriched in the lysate. C_LIO_LIThose Vibrio have been known as pathogen of fish or crustacean. C_LIO_LIViral infection to H. akashiwo can indirectly affect higher trophic-level consumers. C_LI

microbiology↗

bioRxiv2024

A robustly rooted tree of eukaryotes reveals their excavate ancestry.

The eukaryote Tree of Life (eToL) depicts the relationships among all eukaryotic organisms; its root represents the last eukaryotic common ancestor (LECA) from which all extant complex lifeforms are descended. Locating this root is crucial for reconstructing the features of LECA, both as the endpoint of eukaryogenesis and the start-point for the evolution of the myriad complex traits underpinning the diversification of living eukaryotes. However, the position of the root remains contentious due to pervasive phylogenetic artefacts stemming from inadequate evolutionary models, poor taxon sampling, and limited phylogenetic signal. Here, we estimate the root of the eToL with unprecedented resolution based on a new, much larger, dataset of mitochondrial proteins which includes all known eukaryotic supergroups. Our comprehensive analyses with state-of-the-art phylogenetic models reveal that the eukaryotic root lies between two multi-supergroup assemblages: Opimoda+ and Diphoda+. Compellingly, this position is consistently supported across different models and robustness analyses. Notably, groups containing typical excavates are placed on both sides of the root, suggesting the complex features of the excavate cell architecture trace back to LECA. This study is the most comprehensive phylogenetic investigation of the eukaryote root to date, shedding light on the ancestral cells from which extant eukaryotes arose and providing a crucial framework for investigating the origin and evolution of canonical eukaryotic features.

evolutionary biology↗

bioRxiv2023

Phylogenetic diversity of the carbon monoxide-utilizing prokaryotes and their divergent carbon monoxide metabolisms in the human gut microbiome

Although the production of toxic CO within the human body has been detected, only a few CO-utilizing prokaryotes (CO utilizers) have been reported in the human gut, and their phylogenetic and physiological diversity remains unclear. Here, we unveiled more than thousand representative genomes originating from previously unexplored potential CO-utilizing prokaryotes, which contain CO dehydrogenase (CODH) genes. More than half of CODH-bearing prokaryotes possess genes for the autotrophic Wood-Ljungdahl pathway (WLP). However, 79% of these prokaryotes commonly lack a key gene for WLP, which encodes enzyme that synthesizes formate from CO2 and reductants such as H2, suggesting that they share a degenerated WLP. Instead, many were predicted to possess an alternative way of synthesizing formate from pyruvate, which is a product of glycolysis. In addition to degenerated WLP, seven genes neighboring the CODH gene were found, which may reflect diverse utilization of CO in the human gut. Our findings reveal the unique and diverse nature of CO metabolism in the human gut microbiome, suggesting its potential contribution to CO consumption and gut homeostasis. Impact statementCarbon monoxide (CO)-utilizing prokaryotes mitigate the toxic impact of CO by consuming it as energy and/or carbon sources. In addition to various environments, CO is also produced via multiple routes, such as heme degradation, in the human body and accumulates in the gut. Revealing CO-utilizing prokaryotes and their CO metabolisms in the human gut would contribute to gaining insight into how microbial community functions are involved in maintaining human gut homeostasis. Nevertheless, the limited number of CO utilizers in the human gut microbiome have been reported. In our study, a significant proportion of human gut microbial genomes belonging to diverse phyla were revealed to be of potential CO-utilizing prokaryotes. Additionally, the majority of CO-utilizing prokaryote genomes in the human gut have potentially remodeled the Wood- Ljungdahl pathway (WLP), one of the most well-known autotrophic pathways, to the degenerated, heterotrophic form. Moreover, there were seven other genes neighboring CODH in the human gut CO-utilizers, suggesting various CO utilization. Our findings would pave the way for future explorations into microbial metabolic adaptations and their implications for human health. Data summaryThe human gut prokaryote genomes were downloaded from HumGut database (Hiseni et al. 2021; https://arken.nmbu.no/~larssn/humgut/). The accession numbers of CODH/ACS-bearing genomes from environments without host-association (Inoue et al., 2022) are listed in Table S1. Metatranscriptomic datasets were downloaded from the NCBI Sequence Read Archive (SRA) under the Bioproject accession numbers PRJNA354235 and PRJNA707065 and their accession IDs are listed in Table S2.

microbiology↗

bioRxiv2023

Encyclopaedia of DNA polymerases localized in organelles: Contribution of genes from diverse bacteria including the proto-mitochondrion.

DNA polymerases (DNAPs) synthesize DNA from deoxyribonucleotides in a semi-conservative manner and serve as the core of DNA replication and repair machineries. In eukaryotic cells, there are two genome-containing organelles, mitochondria and plastids, that were derived from an -proteobacterium and a cyanobacterium, respectively. Except for rare cases of genome-lacking mitochondria and plastids, both organelles must be served by nucleus-encoded DNAPs that localize and work in them to maintain their genomes. The evolution of organellar DNAPs has yet to be fully understood because of two unsettled issues. First, the diversity of organellar DNAPs has not been elucidated in the full spectrum of eukaryotes. Second, it is unclear when the DNAPs that were used originally in the endosymbiotic bacteria giving rise to mitochondria and plastids were discarded, as the organellar DNAPs known to date show no phylogenetic affinity to those of the extant -proteobacteria or cyanobacteria. In this study, we identified from diverse eukaryotes 134 family A DNAP sequences, which were classified into 10 novel types, and explored their evolutionary origins. The subcellular localizations of selected DNAPs were further examined experimentally. The results presented here suggest that the diversity of organellar DNAPs has been shaped by multiple transfers of the PolI gene from phylogenetically broad bacteria, and their occurrence in eukaryotes was additionally impacted by secondary plastid endosymbioses. Finally, we propose that the last eukaryotic common ancestor may have possessed two mitochondrial DNAPs, POP and a candidate of the direct descendant of the proto-mitochondrial DNAP, rdxPolA, identified in this study.

evolutionary biology↗

bioRxiv2023

Taxonomic difference in marine bloom-forming phytoplanktonic species affects dynamics of both bloom-responding prokaryotes and prokaryotic viruses

The production of dissolved organic matter during phytoplankton blooms and consumption by heterotrophic prokaryotes promotes marine carbon biogeochemical cycling. Although prokaryotic viruses are crucial biological entities, their dynamics during such blooms are not fully understood. Here, we investigated the dynamics of coastal prokaryotic communities and viruses during blooms in a microcosm experiment using dissolved intracellular fractions of taxonomically distinct phytoplankton, the diatom Chaetoceros sp. (CIF) and the raphidophycean alga Heterosigma akashiwo (HIF). Ribosomal RNA gene amplicon and viral metagenomic analyses revealed that particular prokaryotes and prokaryotic viruses specifically increased in either CIF and HIF, indicating that different phytoplankton intracellular fractions promote distinct dynamics of not only prokaryotic community but also prokaryotic viruses. Our microcosm experiments and environmental data mining identified both known and novel possible host-virus pairs. In particular, a growth of phytoplanktonic organic matter-associated prokaryotes, such as Bacteroidetes Polaribacter and NS9 marine group, Vibrio spp., and Rhodobacteriales Nereida and Planktomarina, was accompanied by an increase in viruses predicted to infect Bacteroidetes, Vibrio, and Rhodobacteriales, respectively. Collectively, our findings suggest that elucidating tripartite relationships among phytoplankton, prokaryotes, and prokaryotic viruses would further our understanding of coastal microbial ecosystems. We state that -All the data underlying the study are available at the DNA Data Bank of Japan (DDBJ) under project number PRJDB14359 and accession number DRA014887. -This study was supported by Grants-in-Aid for Scientific Research (No. 16H06429, No. 17H03850, No. 21H05057, and No. 21J14854) from the Japan Society for the Promotion of Science (JSPS). -We have no potential conflicts of interest to declare. -We have read and understood your journals policies, and we believe that neither the manuscript nor the study violates any of these. -We do not use any clinical data, human subjects, or laboratory animals. -None of the materials have been published or are under consideration for publication elsewhere. CRediTHiroaki Takebe: Funding acquisition, conceptualization, investigation, formal analysis, visualization, and writing (original draft). Kento Tominaga: Conceptualization, investigation, and writing (review and editing). Tatsuhiro Isozaki: investigation. Tetsuhiro Watanabe: Resources. Keigo Yamamoto: Resources. Ryoma Kamikawa: Conceptualization, supervision, and writing (review and editing). Takashi Yoshida: Funding acquisition, project administration, conceptualization, supervision, and writing (review and editing).

microbiology↗

bioRxiv2023

Isolation and genomic and physiological characterization of Parageobacillus sp. G301, the isolate capable of both hydrogenogenic and aerobic carbon monoxide oxidation

Prokaryotes, known as carbon monoxide (CO) oxidizers, use CO as the carbon or energy source with CO dehydrogenases (CODHs), which are divided into nickel-containing CODH (Ni-CODH) that are sensitive to O2 and molybdenum-containing CODH (Mo-CODH) that are capable of aerobic functioning. The oxygen conditions for CO oxidizers to oxidize CO may be limited because CO oxidizers isolated and characterized so far have either Ni- or Mo-CODH. Here, we report a novel CO oxidizer capable of CO oxidation with both types of CODH based on genomic and physiological characterization of the isolate Parageobacillus sp. G301. This thermophilic facultative anaerobic Bacillota bacterium was isolated from the sediment of a freshwater lake. Genomic analyses showed that G301 was the only isolate possessing both Ni-CODH and Mo-CODH. Genome-based reconstruction of the respiratory machinery and physiological investigation indicated that CO oxidation by Ni-CODH was coupled with H2 production (proton reduction), and CO oxidation by Mo-CODH was coupled with O2 reduction under aerobic conditions and nitrate reduction under anaerobic conditions. G301 would thus be able to thrive via CO oxidation under a wide range of conditions, from aerobic environments to anaerobic environments even without terminal electron acceptors other than protons. As comparative genome analyses revealed no significant differences in genome structures and encoded cellular functions, except for CO oxidation between CO oxidizers and non-CO oxidizers in the genus Parageobacillus, CO oxidation genes would be retained exclusively for CO metabolism and related respiration. ImportanceMicrobial CO oxidation has received a lot of attention because it contributes to global carbon cycling in addition to functioning as a remover of CO, which is toxic to many organisms. Microbial CO oxidizers have a punctate phylogenetic distribution throughout bacteria and archaea, even in genus-level monophyletic groups. In this study, we demonstrated that the new isolate Parageobacillus sp. G301 is capable of both anaerobic (hydrogenogenic) and aerobic CO oxidation, which had not been previously reported. The discovery of this new isolate, which is versatile in CO metabolism, would accelerate research into such CO oxidizers with diverse CO metabolisms, expanding our understanding of microbial diversity. Through comparative genomic analyses, we propose that CO oxidation genes are optional but not essential genetic elements in the genus Parageobacillus, providing insight into a factor that shapes the mosaic phylogenetic distribution of CO oxidizers, even in genus-level monophyletic groups.

microbiology↗

bioRxiv2022

Proton-pumping rhodopsins in marine diatoms

Diatoms are a major phytoplankton group responsible for about 20% of Earths primary production. They carry out photosynthesis inside the plastid, an organelle obtained through eukaryote-eukaryote endosymbiosis. Recently, microbial rhodopsin, a photoreceptor distinct from chlorophyll-based photosystems, has been identified in certain diatoms. However, the physiological function of diatom rhodopsin is not well understood. Here we show that the diatom rhodopsin acts as a light-driven proton pump and localizes to the outermost membrane of the four membrane-bound complex plastids. Heterologous expression techniques were used to investigate the protein function and subcellular localization of diatom rhodopsin. Using model simulations, we further evaluated the physiological role of the acidic pool in the plastid produced by proton-transporting rhodopsin. Our results propose that the rhodopsin-derived acidic pool may be involved in a photosynthetic CO2-concentrating mechanism and assist CO2 fixation in diatom cells.

microbiology↗

bioRxiv2021

Genome evolution of a non-parasitic secondary heterotroph, the diatom Nitzschia putrida

Secondary loss of photosynthesis is observed across almost all plastid-bearing branches of the eukaryotic tree of life. However, genome-based insights into the transition from a phototroph into a secondary heterotroph have so far only been revealed for parasitic species. Free-living organisms can yield unique insights into the evolutionary consequence of the loss of photosynthesis, as the parasitic lifestyle requires specific adaptations to host environments. Here we report on the diploid genome of the free-living diatom Nitzschia putrida (35 Mbp), a non-photosynthetic osmotroph whose photosynthetic relatives contribute ca. 40% of net oceanic primary production. Comparative analyses with photosynthetic diatoms revealed that a combination of genes loss, the horizontal acquisition of genes involved in organic carbon degradation, a unique secretome and the rapid divergence of conserved gene families involved in cell wall and extracellular metabolism appear to have facilitated the lifestyle of a non-parasitic, free-living secondary heterotroph.

genomics↗

bioRxiv2019

Large DNA virus promoted the endosymbiotic evolution to make a photosynthetic eukaryote

Chloroplasts in photosynthetic eukaryotes originated from a cyanobacterial endosymbiosis far more than 1 billion years ago1-3. Due to this ancientness, it remains unclear how this evolutionary process proceeded. To unveil this mystery, we analysed the whole genome sequence of a photosynthetic rhizarian amoeba4, Paulinella micropora5,6, which has a chloroplast-like organelle that originated from another cyanobacterial endosymbiosis7-10 about 0.1 billion years ago11. Here we show that the predacious amoeba that engulfed cyanobacteria evolved into a photosynthetic organism very quickly in the evolutionary time scale, probably aided by the drastic genome reorganization activated by large DNA virus. In the endosymbiotic evolution of eukaryotic cells, gene transfer from the endosymbiont genome to the host nucleus is essential for the evolving host cell to control the endosymbiont-derived organelle12. In P. micropora, we found that the gene transfer from the free-living and endosymbiotic bacteria to the amoeba nucleus was rapidly activated but both simultaneously ceased within the initiation period of the endosymbiotic evolution, suggesting that the genome reorganization drastically proceeded and completed. During this period, large DNA virus appeared to have infected the amoeba, followed by the rapid amplification and diversification of virus-related genes. These findings led us to re-examine the conventional endosymbiotic evolutionary scenario that exclusively deals with the host and the symbiont, and to extend it by incorporating a third critical player, large DNA virus, which activates the drastic gene transfer and genome reorganization between them. This Paulinella version of the evolutionary hypothesis deserves further testing of its generality in evolutionary systems and could shed light on the unknown roles of large DNA viruses13 in the evolution of terrestrial life.

evolutionary biology↗

bioRxiv2019

Dinoflagellates with relic endosymbiont nuclei as novel models for elucidating organellogenesis

Nucleomorphs are relic endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process integrating an endosymbiont alga into be a host-governed plastid (organellogenesis). Nevertheless, past studies suggested that DNA transfer from the endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which from-endosymbiont-to-host DNA transfer is on-going and of which endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide the evidence for the presence of DNA in the two nucleomorphs and transfer of endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. Combined, we conclude that the host-endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as new models for elucidating organellogenesis.

evolutionary biology↗

bioRxiv2017

Phylogenomics places orphan protistan lineages in a novel eukaryotic super-group

Recent phylogenetic analyses position certain orphan protist lineages deep in the tree of eukaryotic life, but their exact placements are poorly resolved. We conducted phylogenomic analyses that incorporate deeply sequenced transcriptomes from representatives of collodictyonids (diphylleids), rigifilids, Mantamonas and ancyromonads (planomonads). Analyses of 351 genes, using site-heterogeneous mixture models, strongly support a novel supergroup-level clade that includes collodictyonids, rigifilids and Mantamonas, which we name CRuMs. Further, they robustly place CRuMs as the closest branch to Amorphea (including animals and fungi). Ancyromonads are strongly inferred to be more distantly related to Amorphea than are CRuMs. They emerge either as sister to malawimonads, or as a separate deeper branch. CRuMs and ancyromonads represent two distinct major groups that branch deeply on the lineage that includes animals, near the most commonly inferred root of the eukaryote tree. This makes both groups crucial in examinations of the deepest-level history of extant eukaryotes.

evolutionary biology↗