A Micrarchaeon Isolate Is Covered by a Proteinaceous S-Layer

Gfrerer, Sabrina; Winkler, Dennis C.; Ducassou, Julia Novion; Couté, Yohann; Rachel, Reinhard; Gescher, Johannes

doi:10.1128/aem.01553-21

Cited by 7 publications

(12 citation statements)

References 75 publications

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“…The proteins of the S-layer and archaellin are likely to be highly glycosylated, which could serve as the targets for attachment by strain MJ1 T . The S-layer lattice symmetry and constant of strain MJ1 T are different from those of its host archaeon MJ1HA and even the other reported DPANN archaea (18,19). Strain MJ1 T possesses no obvious homologs to known S-layer proteins.…”

Section: A Hypothetical Model Of Cell Surfaces and Symbiosismentioning

confidence: 77%

“…1H-J; Fig. S3), which seems to be different from the hexagonal lattice (p3/p6) of 'Nanoarchaeum equitans' and 'Micrarchaeum harzensis' (4,18,19).…”

Section: Electron Microscopymentioning

confidence: 83%

“…This is not surprising, given that amino acid sequence identities of S-layer proteins are generally low among archaea in genus or higher taxonomic levels (60). No S-layer proteins have been determined for the DPANN archaea, although several candidates have been proposed (12, 13, 19, 20). We surveyed putative cell-wall or extracellular proteins with signal peptides (Table 1), and found many N-glycosylation sites, but no O-glycosylation sites, in the putative cell surface or extracellular proteins from the MJ1 T genes as described below.…”

Section: Resultsmentioning

confidence: 99%

“…The archaeal S-layer exhibits either oblique (p1 and p2), square (p4), or hexagonal (p3 and p6) lattice symmetry (16). In particular, the S-layers of ‘ Nanoarchaeum equitans’ and ‘Micrarchaeum harzensis’ in the DPANN clade have been reported to represent a hexagonal lattice (p3/p6) (4, 18, 19). Putative genes encoding S-layer proteins have been identified in the genomes of ‘ Nanoarchaeum equitans’ (NEQ300) (20) and ‘Micrarchaeum harzensis’ (Micr_00292) (19).…”

Section: Introductionmentioning

confidence: 99%

“…In particular, the S-layers of ‘ Nanoarchaeum equitans’ and ‘Micrarchaeum harzensis’ in the DPANN clade have been reported to represent a hexagonal lattice (p3/p6) (4, 18, 19). Putative genes encoding S-layer proteins have been identified in the genomes of ‘ Nanoarchaeum equitans’ (NEQ300) (20) and ‘Micrarchaeum harzensis’ (Micr_00292) (19). Indeed, these genes are highly expressed in the transcriptomes and proteomes of the two DPANN archaea (10, 21, 22).…”

Section: Introductionmentioning

confidence: 99%

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Cell surface architecture of the cultivated DPANN archaeonNanobdella aerobiophila

Kato,

Tahara,

Nishimura

et al. 2023

Preprint

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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 archaeonNanobdella aerobiophilastrain MJ1Tand its hostMetallosphaera sedulastrain 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 MJ1Twere different from those of the host archaeon strain MJ1HA. Genomic and transcriptomic analyses highlighted the most highly expressed MJ1Tgene 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°C indicated that cell complexes of strains MJ1Tand MJ1HA were motile, but sole MJ1Tcells were not. Taken together, we propose a model of the symbiotic interaction and cell cycle ofNanobdella 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 ofNanobdella aerobiophila, which will enhance our understanding of the enigmatic physiology and ecological significance of DPANN archaea.

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Section: A Hypothetical Model Of Cell Surfaces and Symbiosismentioning

confidence: 77%

“…1H-J; Fig. S3), which seems to be different from the hexagonal lattice (p3/p6) of 'Nanoarchaeum equitans' and 'Micrarchaeum harzensis' (4,18,19).…”

Section: Electron Microscopymentioning

confidence: 83%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Cell surface architecture of the cultivated DPANN archaeonNanobdella aerobiophila

Kato,

Tahara,

Nishimura

et al. 2023

Preprint

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The importance of biofilm formation for cultivation of a Micrarchaeon and its interactions with its Thermoplasmatales host

et al. 2022

Self Cite

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Micrarchaeota is a distinctive lineage assigned to the DPANN archaea, which includes poorly characterised microorganisms with reduced genomes that likely depend on interactions with hosts for growth and survival. Here, we report the enrichment of a stable co-culture of a member of the Micrarchaeota (Ca. Micrarchaeum harzensis) together with its Thermoplasmatales host (Ca. Scheffleriplasma hospitalis), as well as the isolation of the latter. We show that symbiont-host interactions depend on biofilm formation as evidenced by growth experiments, comparative transcriptomic analyses and electron microscopy. In addition, genomic, metabolomic, extracellular polymeric substances and lipid content analyses indicate that the Micrarchaeon symbiont relies on the acquisition of metabolites from its host. Our study of the cell biology and physiology of a Micrarchaeon and its host adds to our limited knowledge of archaeal symbioses.

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Microbial ecology of the deep terrestrial subsurface

Beaver,

Neufeld

2024

The ISME Journal

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The terrestrial subsurface hosts diverse microbial communities that, collectively, are predicted to comprise as many microbial cells as global surface soils. Although initially thought to be associated with deposited organic matter, contemporary research demonstrates that deep subsurface microbial communities are supported by chemolithoautotrophic primary production, with hydrogen serving as an important source of electrons. Despite recent progress, relatively little is known about the deep terrestrial subsurface compared to more commonly studied environments. Understanding the composition of deep terrestrial subsurface microbial communities and the factors that influence them is of importance because of human-associated activities including long-term storage of used nuclear fuel, carbon capture, and storage of hydrogen for use as an energy vector. In addition to identifying deep subsurface microorganisms, recent research focuses on identifying the roles of microorganisms in subsurface communities, as well as elucidating myriad interactions – syntrophic, episymbiotic, and viral – that occur among community members. In recent years, entirely new groups of microorganisms (i.e., CPR bacteria and DPANN archaea) have been discovered in deep terrestrial subsurface environments, suggesting that much remains unknown about this biosphere. This review explores the historical context for deep terrestrial subsurface microbial ecology and highlights recent discoveries that shape current ecological understanding of this poorly explored microbial habitat. Additionally, we highlight the need for multifaceted experimental approaches to observe phenomena such as cryptic cycles, complex interactions, and episymbiosis, which may not be apparent when using single approaches in isolation, but are nonetheless critical to advancing our understanding of this deep biosphere.

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A Micrarchaeon Isolate Is Covered by a Proteinaceous S-Layer

Cited by 7 publications

References 75 publications

Cell surface architecture of the cultivated DPANN archaeonNanobdella aerobiophila

Cell surface architecture of the cultivated DPANN archaeonNanobdella aerobiophila

The importance of biofilm formation for cultivation of a Micrarchaeon and its interactions with its Thermoplasmatales host

Microbial ecology of the deep terrestrial subsurface

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