bioRxiv Science⌕ Search

Biology subjects

Uematsu, K.

Publications and source records attributed to Uematsu, K..

8 recordsLinked to original sources

Eukaryotes' closest relatives are internally simple syntrophic archaea

Eukaryotes are theorized to have originated from an archaeal phylum Promethearchaeota (formerly Asgard archaea)1,2. The first cultured representatives revealed valuable insight3,4 but are distantly related to the first eukaryotic common ancestor (FECA), leaving many unknowns regarding this archaeons biology. Here, we report isolation of two strains belonging to the order proposed as FECAs closest relative, Hodarchaeales,5 as members of a pure co- and tri-culture with methanogenic partners. Both are obligately anaerobic, syntrophic, peptide-degrading, and mesophilic archaea that have simple internal cell structure and produce protrusions and vesicles, like Promethearchaeales3,4. All strains demonstrate behavior focused on cell construction rather than division, unlike typical prokaryotes6. Strain HC1 possesses genes associated with aerobic lifestyles but lacks complete pathways for aerobic respiration and co-cultures cannot grow under (micro)aerobic conditions, suggesting the genes support oxygen detoxification rather than respiration. Reflecting this, HC1 can survive and grow under microaerobic conditions only when aerobic organisms are present. Phylogenetic analyses indicate FECA may have possessed these genes and thus some aerotolerance. Physiological, genomic, and phylogenetic observations indicate FECA was a simple-celled anaerobic syntrophic peptide-degrading archaeon with a non-growth-centric lifestyle and potential adaptations towards an oxygenated planet--the archaea-eukaryote transition was steep in both cell structure and aerobiosis.

microbiology↗

The kin-selected context of duelling in horned aphids: cooperation or conflict?

In one-on-one (dyadic) contests in group-living animals, relatedness is of potentially critical importance in determining the relative value of the resources for which the individuals are fighting. We investigated the function of dyadic contests over access to a food resource (plant phloem) in the horned aphid Astegopteryx bambusae, by observing competing aphids in the field and genotyping them with microsatellite markers. Each aphid colony consists of a small number of clones, creating levels of relatedness that can be both high and variable. The contests involve only low costs in terms of time or injury. Our results indicate that there is no kin-discrimination in the duelling pairs of aphids. Genetic relatedness between duelling pairs did not differ significantly from that of randomly selected pairs and showed no association with contest duration or outcome. The mean relatedness between a duelling pair was 0.79 {+/-} 0.12 (mean {+/-} SD, N = 75), with 56% (42/75) of duels occurring between clonal pairs. We suggest that the duels in these Astegopteryx aphids are not an aggressive fight for resources between different genotypes, but rather a low-cost method by which the aphids assess each others reproductive value. 83% (50/60) of the contests between aphids of different ages were won by the aphid that was older, and therefore of greater reproductive value, providing an indirect fitness benefit for the losing younger individual. Younger nymphs, when attacked by older aphids, yield feeding sites altruistically and gain inclusive fitness benefits: this provides a compelling selective context for the evolution of the young, rather than old, altruistic soldiers that are observed in the open colonies of many cerataphidine species.

ecology↗

Cell surface architecture of the cultivated DPANN archaeon Nanobdella aerobiophila

The DPANN archaeal clade includes obligately ectosymbiotic species. Their cell surfaces potentially play an important role in the symbiotic interaction between the ectosymbionts and their hosts. However, little is known about the mechanism of the ectosymbiosis. Here, we show cell surface structures of the cultivated DPANN archaeon Nanobdella aerobiophila strain MJ1T and its host Metallosphaera sedula strain MJ1HA, using a variety of electron microscopy techniques, i.e., negative-staining transmission electron microscopy (TEM), quick-freeze deep-etch (QFDE) TEM, and 3D electron tomography. The thickness, unit size, and lattice symmetry of the S-layer of strain MJ1T were different from those of the host archaeon strain MJ1HA. Genomic and transcriptomic analyses highlighted the most highly expressed MJ1T gene for a putative S-layer protein with multiple glycosylation sites and immunoglobulin-like folds, which has no sequence homology to known S-layer proteins. In addition, genes for putative pectin lyase- or lectin-like extracellular proteins, which are potentially involved in symbiotic interaction, were found in the MJ1T genome based on in silico 3D protein structure prediction. Live cell imaging at the optimum growth temperature of 65{degrees}C indicated that cell complexes of strains MJ1T and MJ1HA were motile, but sole MJ1T cells were not. Taken together, we propose a model of the symbiotic interaction and cell cycle of Nanobdella aerobiophila. ImportanceDPANN archaea are widely distributed in a variety of natural and artificial environments, and may play a considerable role in the microbial ecosystem. All of the cultivated DPANN archaea so far need host organisms for their growth, i.e., obligately ectosymbiotic. However, the mechanism of the ectosymbiosis by DPANN archaea is largely unknown. To this end, we performed a comprehensive analysis of the cultivated DPANN archaeon, Nanobdella aerobiophila, using electron microscopy, live cell imaging, transcriptomics, and genomics including 3D protein structure prediction. Based on the results, we propose a reasonable model of the symbiotic interaction and cell cycle of Nanobdella aerobiophila, which will enhance our understanding of the enigmatic physiology and ecological significance of DPANN archaea.

microbiology↗

Eusocial evolution without a nest: kin structure of social aphids forming open colonies on bamboo

Living in nests is an almost universal feature of eusocial animals. In some aphids, however, sterile soldier castes have evolved in open colonies without a nest. To clarify the factors promoting the evolution of eusociality in these colonies, we used newly developed microsatellite markers to compare the kin structure of the open colonies of two aphid species on bamboo: the non-eusocial colonies of Astegopteryx bambucifoliae and the eusocial colonies of Pseudoregma alexanderi on Dendrocalamus latiflorus. Our samples, from over 1,000 hectares, contained 99 clones of A. bambucifoliae and 19 of P. alexanderi. Clonal mixing occurred in both species: average pairwise relatedness within a colony was 0.54 in A. bambucifoliae and 0.71 in P. alexanderi. Each clone of A. bambucifoliae occurred in a unique location, whereas those of P. alexanderi occurred in multiple locations and more than 90% of individuals came from just four clones. There was significant genetic variation among different colonies in the same clump (stem-cluster) in A. bambucifoliae but not in P. alexanderi, indicating that P. alexanderi colonies in a single clump are genetically homogenized, functioning as a large colony. In P. alexanderi, the proportion of sterile soldiers to normal first-instar nymphs was significantly different across the four clones. Our results indicate that the lack of input of migrants from the primary host and feeding on a large, stable host plant are important ecological factors that might favour the evolution of eusociality, enabling the production of genetically homogenised, large, and long-lived colonies. After eusociality evolves on the secondary host, the optimal strategy of soldier production might vary between different clones. Significance StatementNest-living has often been considered to be a necessary condition for the evolution of eusociality. In a small number of aphid species, however, sterile soldier castes have evolved in open colonies without a nest. To understand why these aphids are unique, we examined the kin structure and genetic relatedness of individuals within eusocial and non-eusocial open colonies of two aphid species on bamboo. We found that clonal mixing occurred in both species, but the eusocial colonies are more genetically homogenized, functioning as a large colony. Our results suggest that ecological conditions that promote genetically homogenized, large and long-lived colonies are important for the evolution of eusociality in these aphids. We propose that the open colonies of social aphids provide an ideal model system in which to study the evolution of altruism.

evolutionary biology↗

Seasonal polyphenism underlies the origin of a sterile caste in aphids

The origin of a sterile caste among eusocial animals has been a fundamental but still unresolved problem in understanding the evolution of biological complexity. At the origin of a sterile caste, recruitment of pre-existing plasticity may lead to produce physiologically, morphologically and behaviorally distinct caste phenotypes. Here, we provide convincing evidence that preexisting seasonal polyphenism has been recruited to generate a sterile soldier caste in host-alternating social aphids. We demonstrate that sterile soldier nymphs of Colophina aphids resemble those of monomorphic defensive nymphs produced in a different host-plant generation. Notably, the two morphs in the basal species show the closest similarity in morphology and gene expression among all morph pairs. Moreover, their evolutionary phenotypic changes along the phylogeny of four Colophina species are significantly correlated positively. These results suggest that they may share the common regulatory mechanisms of development, which underpin the heterochronic expression of monomorphic defenders on the different host plant leading to the evolution of a novel soldier phenotype. We further demonstrate that the monomorphic defenders can increase their inclusive fitness by killing predators eggs on a seasonally different host plant. Taken together, our findings suggest that preexisting plasticity that can gain indirect fitness benefits facilitates the early evolution of a sterile caste.

evolutionary biology↗

A Novel Bacterial Speciation Process Observed in a Symbiotic Marine Population

Incomplete lineage sorting (ILS), where ancestral polymorphisms persist through rapid speciation, is a hallmark of eukaryotic radiations but undocumented in prokaryotes. We report ILS associated speciation in the globally distributed marine bacterium Sulfitobacter, analyzing 74 strains from 16 oceanic regions and 15 ecosystem types. Genomic analysis resolved over ten genetically monomorphic clades sharing near uniform whole genome divergence (average nucleotide identity {approx}95%). However, individual genes and even adjacent nucleotide sites support conflicting phylogenetic relationships among clades. The median length of nearly identical sequence blocks supporting alternative topologies is less than 50 base pairs, far shorter than typical adaptive cassettes. This within gene, site level discordance provides a diagnostic signature of ancestral polymorphism retention following rapid fragmentation, ruling out adaptive gene sweeps. Demographic inference places this radiation on a timescale of tens of millennia, 100 to 1,000 fold faster than eukaryotic ILS, and traces the clades to a hyper polymorphic, highly recombining ancestor. Neutral simulations show that transient mutation surges or population bottlenecks alone can generate this pattern, without adaptive selection or ecological partitioning. By bridging eukaryotic and prokaryotic speciation paradigms, our findings demonstrate that ILS, previously considered exclusive to sexual eukaryotes, can drive rapid, neutral diversification in bacteria, expanding the mechanisms known to generate prokaryotic biodiversity.

microbiology↗

Defensive nymphs in the water-repellent gall of the social aphid Colophina monstrifica (Hemiptera: Aphididae: Eriosomatinae)

The aphid Colophina monstrifica forms woolly colonies with sterile soldiers on the secondary host Clematis uncinata in Taiwan. However, the gall or primary-host generation of C. monstrifica has not been found to date. We successfully induced galls of the species on trees of Zelkova serrata through attaching its eggs onto the trees, and also found a few naturally formed galls on another Z. serrata tree. The identity of the aphids was confirmed by examining their morphology and mitochondrial DNA sequences. First- and second-instar nymphs in the galls exhibited attacking behavior toward artificially introduced moth larvae. Observations with a scanning electron microscope revealed that the gall inner surface was densely covered with minute trichomes. This indicates the water repellency of the inner surface, and strongly suggests that young nymphs of C. monstrifica dispose of honeydew globules outside the gall, as known in the congener C. clematis.

zoology↗

Isolation of an archaeon at the prokaryote-eukaryote interface

The origin of eukaryotes remains enigmatic. Current data suggests that eukaryotes may have risen from an archaeal lineage known as \"Asgard archaea\". Despite the eukaryote-like genomic features found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear due to the lack of cultured representatives and corresponding physiological insight. Here we report the decade-long isolation of a Lokiarchaeota-related Asgard archaeon from deep marine sediment. The archaeon, \"Candidatus Prometheoarchaeum syntrophicum strain MK-D1\", is an anaerobic, extremely slow-growing, small cocci ([~]550 nm), that degrades amino acids through syntrophy. Although eukaryote-like intracellular complexities have been proposed for Asgard archaea, the isolate has no visible organella-like structure. Ca. P. syntrophicum instead displays morphological complexity - unique long, and often, branching protrusions. Based on cultivation and genomics, we propose an \"Entangle-Engulf-Enslave (E3) model\" for eukaryogenesis through archaea-alphaproteobacteria symbiosis mediated by the physical complexities and metabolic dependency of the hosting archaeon.

microbiology↗