Termites thrive on dead plant matters with the aid of microorganisms resident in their gut. The gut microbiota comprises protists (single-celled eukaryotes), bacteria, and archaea, most of which are ...unique to the termite gut ecosystem. Although this symbiosis has long been intriguing researchers of both basic and applied sciences, its detailed mechanism remains unclear due to the enormous complexity and the unculturability of the microbiota. In the effort to overcome the difficulty, recent advances in omics, such as metagenomics, metatranscriptomics, and metaproteomics have gradually unveiled the black box of this symbiotic system. Genomics targeting a single species of the unculturable microbial members has also provided a great progress in the understanding of the symbiotic interrelationships among the gut microorganisms. In this review, the symbiotic system organized by wood-feeding termites and their gut microorganisms is outlined, focusing on the recent achievement in omics studies of this multilayered symbiotic system.
Termites play a key role in the global carbon cycle as decomposers. Their ability to thrive solely on dead plant matter is chiefly attributable to the activities of gut microbes, which comprise ...protists, bacteria, and archaea. Although the majority of the gut microbes are as yet unculturable, molecular analyses have gradually been revealing their diversity and symbiotic mechanisms. Culture-independent studies indicate that a single termite species harbors several hundred species of gut microbes unique to termites, and that the microbiota is consistent within a host termite species. To elucidate the functions of these unculturable symbionts, environmental genomics has recently been applied. Particularly, single-species-targeting metagenomics has provided a breakthrough in the understanding of symbiotic roles, such as the nitrogen fixation, of uncultured, individual microbial species. A combination of single-species-targeting metagenomics, conventional metagenomics, and metatranscriptomics should be a powerful tool to dissect this complex, multi-layered symbiotic system.
During the course of the evolution of endosymbiotic organelles, mitochondria and plastids, numerous genes were transferred from ancestral organelles and other bacteria to the host genome. This ...process required, firstly, incorporating DNA fragments encoding intact genes into the host genome, secondly, acquiring the expression signals such as eukaryotic promoters and regulatory elements that enable their transcription in eukaryotic hosts, and thirdly, in many cases, evolving a dedicated targeting system to transport and import their protein products into the endosymbiotic organelles 1. The advent of this protein-targeting machinery is commonly assumed to be the most crucial step, at which point an endosymbiont becomes an organelle 2,3. Bacterial lineages have repeatedly evolved intimate symbioses with eukaryotic hosts, but the establishment of the protein translocation system has been shown only in the cases of bona fide organelles and the photosynthetic symbiosis in a cercozoan amoeba 3. Here, we report that an aphid gene that was horizontally acquired from a bacterium produces protein, which is transported to an obligate intracellular bacterial symbiont. To our knowledge, this is the first report of integration between multicellular eukaryotes and bacteria to the extent of ‘organellogenesis’.
Nakabachi et al. demonstrate that a protein encoded in the aphid genome is transported into Buchnera symbionts. As transport of host-encoded proteins to organelles is a defining feature of organelles, this work suggests that the division between organelles and symbionts may not be so clear cut.
A novel type of agarose gel microcapsule (AGM), consisting of an alginate picolitre sol core and an agarose gel shell, was developed to obtain high-quality, single-cell, amplified genomic DNA of ...bacteria. The AGM is easy to prepare in a stable emulsion with oil of water-equivalent density, which prevents AGM aggregation, with only standard laboratory equipment. Single cells from a pure culture of Escherichia coli, a mock community comprising 15 strains of human gut bacteria, and a termite gut bacterial community were encapsulated within AGMs, and their genomic DNA samples were prepared with massively parallel amplifications in a tube. The genome sequencing did not need second-round amplification and showed an average genome completeness that was much higher than that obtained using a conventional amplification method on the microlitre scale, regardless of the genomic guanine-cytosine content. Our novel method using AGM will allow many researchers to perform single-cell genomics easily and effectively, and can accelerate genomic analysis of yet-uncultured microorganisms.
The fidelity of vertical transmission is a critical factor in maintaining mutualistic associations with microorganisms. The obligate mutualism between termites and intestinal protist communities has ...been maintained for over 130 million years, suggesting the faithful transmission of diverse protist species across host generations. Although a severe bottleneck can occur when alates disperse with gut protists, how protist communities are maintained during this process remains largely unknown. In this study, we examined the dynamics of intestinal protist communities during adult eclosion and alate dispersal in the termite
. We found that the protist community structure in last-instar nymphs differed significantly from that in workers and persisted intact during adult eclosion, whereas all protists disappeared from the gut during moults between worker stages. The number of protists in nymphs and alates was substantially lower than in workers, whereas the proportion of protist species exhibiting low abundance in workers was higher in nymphs and alates. Using a simulation-based approach, we demonstrate that such changes in the protist community composition of nymphs and alates improve the transmission efficiency of whole protist species communities. This study thus provides novel insights into how termites have maintained mutualistic relationships with diverse gut microbiota for generations.
The evolutionary processes that drive variation in genome size across the tree of life remain unresolved. Effective population size (Ne) is thought to play an important role in shaping genome size ...1–3—a key example being the reduced genomes of insect endosymbionts, which undergo population bottlenecks during transmission 4. However, the existence of reduced genomes in marine and terrestrial prokaryote species with large Ne indicate that genome reduction is influenced by multiple processes 3. One candidate process is enhanced mutation rate, which can increase adaptive capacity but can also promote gene loss. To investigate evolutionary forces associated with prokaryotic genome reduction, we performed molecular evolutionary and phylogenomic analyses of nine lineages from five bacterial and archaeal phyla. We found that gene-loss rate strongly correlated with synonymous substitution rate (a proxy for mutation rate) in seven of the nine lineages. However, gene-loss rate showed weak or no correlation with the ratio of nonsynonymous/synonymous substitution rate (dN/dS). These results indicate that genome reduction is largely associated with increased mutation rate, while the association between gene loss and changes in Ne is less well defined. Lineages with relatively high dS and dN, as well as smaller genomes, lacked multiple DNA repair genes, providing a proximate cause for increased mutation rates. Our findings suggest that similar mechanisms drive genome reduction in both intracellular and free-living prokaryotes, with implications for developing a comprehensive theory of prokaryote genome size evolution.
•Mutation rate is correlated with gene loss in multiple prokaryotic lineages•Changes in effective population size are weakly associated with gene loss•Increased mutation rates should be considered in theories of genome-size evolution
Using phylogenomic analyses, Bourguignon et al. show gene loss and DNA substitution rates (dN, dS) are correlated in seven of nine prokaryote lineages examined. In contrast, gene loss rate is weakly associated with dN/dS. These results indicate that mutation rate, rather than effective population size, is a key driver of genome reduction in prokaryotes.
Several Trichonympha protist species in the termite gut have independently acquired Desulfovibrio ectosymbionts in apparently different stages of symbiosis. Here, we obtained the near-complete genome ...sequence of Desulfovibrio phylotype ZnDsv-02, which attaches to the surface of Trichonympha collaris cells, and compared it with a previously obtained genome sequence of 'Candidatus Desulfovibrio trichonymphae' phylotype Rs-N31, which is almost completely embedded in the cytoplasm of Trichonympha agilis. Single-nucleotide polymorphism analysis indicated that although Rs-N31 is almost clonal, the ZnDsv-02 population on a single host cell is heterogeneous. Despite these differences, the genome of ZnDsv-02 has been reduced to 1.6 Mb, which is comparable to that of Rs-N31 (1.4 Mb), but unlike other known ectosymbionts of protists with a genome similar in size to their free-living relatives. Except for the presence of a lactate utilization pathway, cell-adhesion components and anti-phage defense systems in ZnDsv-02, the overall gene-loss pattern between the two genomes is very similar, including the loss of genes responsive to environmental changes. Our study suggests that genome reduction can occur in ectosymbionts, even when they can be transmitted horizontally and obtain genes via lateral transfer, and that the symbiont genome size depends heavily on their role in the symbiotic system.
The Palaeognathae comprise the flightless ratites and the volant tinamous, and together with the Neognathae constitute the extant members of class Aves. It is commonly believed that Palaeognathae ...originated in Gondwana since most of the living species are found in the Southern Hemisphere 1–3. However, this hypothesis has been questioned because the fossil paleognaths are mostly from the Northern Hemisphere in their earliest time (Paleocene) and possessed many putative ancestral characters 4. Uncertainties regarding the origin and evolution of Palaeognathae stem from the difficulty in estimating their divergence times 1, 2 and their remarkable morphological convergence. Here, we recovered nuclear genome fragments from extinct elephant birds, which enabled us to reconstruct a reliable phylogenomic time tree for the Palaeognathae. Based on the tree, we identified homoplasies in morphological traits of paleognaths and reconstructed their morphology-based phylogeny including fossil species without molecular data. In contrast to the prevailing theories, the fossil paleognaths from the Northern Hemisphere were placed as the basal lineages. Combined with our stable divergence time estimates that enabled a valid argument regarding the correlation with geological events, we propose a new evolutionary scenario that contradicts the traditional view. The ancestral Palaeognathae were volant, as estimated from their molecular evolutionary rates, and originated during the Late Cretaceous in the Northern Hemisphere. They migrated to the Southern Hemisphere and speciated explosively around the Cretaceous-Paleogene boundary. They then extended their distribution to the Gondwana-derived landmasses, such as New Zealand and Madagascar, by overseas dispersal. Gigantism subsequently occurred independently on each landmass.
•Nuclear genome fragments from extinct elephant bird species were recovered•A stable phylogenomic time tree for the Palaeognathae was inferred•A Laurasian origin of Palaeognathae is supported by molecular and morphological data•Ancestral paleognaths had small body size (∼3.5–5 kg) and probably were volant
Yonezawa et al. recover nuclear genome fragments from extinct elephant birds and reconstruct a stable phylogenomic time tree for the Palaeognathae. Their tree based on morphological characters places the fossil paleognaths from the Northern Hemisphere as the basal lineages. This evidence suggests a Laurasian origin of Palaeognathae.
Cryoconites are microbial aggregates commonly found on glacier surfaces where they tend to take spherical, granular forms. While it has been postulated that the microbes in cryoconite granules play ...an important role in glacier ecosystems, information on their community structure is still limited, and their functions remain unclear. Here, we present evidence for the occurrence of nitrogen cycling in cryoconite granules on a glacier in Central Asia. We detected marker genes for nitrogen fixation, nitrification and denitrification in cryoconite granules by digital polymerase chain reaction (PCR), while digital reverse transcription PCR analysis revealed that only marker genes for nitrification and denitrification were abundantly transcribed. Analysis of isotope ratios also indicated the occurrence of nitrification; nitrate in the meltwater on the glacier surface was of biological origin, while nitrate in the snow was of atmospheric origin. The predominant nitrifiers on this glacier belonged to the order Nitrosomonadales, as suggested by amoA sequences and 16S ribosomal RNA pyrosequencing analysis. Our results suggest that the intense carbon and nitrogen cycles by nitrifiers, denitrifiers and cyanobacteria support abundant and active microbes on the Asian glacier.
Centrioles are cylindrical microtubule-based structures whose assembly is critical for the formation of cilia, flagella, and centrosomes. The centriole proximal region harbors a cartwheel that ...dictates the 9-fold symmetry of centrioles. Although the cartwheel architecture has been recently analyzed, how it connects to the peripheral microtubules is not understood. More generally, a high-resolution view of the proximal region of the centriole is lacking, thus limiting understanding of the underlying assembly mechanisms.
We report the complete architecture of the Trichonympha centriole proximal region using cryotomography. The resulting 3D map reveals several features, including additional densities in the cartwheel that exhibit a 9-fold symmetrical arrangement, as well as the structure of the Pinhead and the A-C linker that connect to microtubules. Moreover, we uncover striking chiral features that might impart directionality to the entire centriole. Furthermore, we identify Trichonympha SAS-6 and demonstrate that it localizes to the cartwheel in vivo.
Our work provides unprecedented insight into the architecture of the centriole proximal region, which is key for a thorough understanding of the mechanisms governing centriole assembly.
•Complete architecture of Trichonympha proximal centriole•The CID might facilitate 9-fold symmetrization of the cartwheel•The Pinhead and the A-C linker exhibit chiral features•TaSAS-6 assembles into rings in the cartwheel
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