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

Krause, Susanne; Gfrerer, Sabrina; Kügelgen, Andriko von; Reuse, Carsten; Dombrowski, Nina; Villanueva, Laura; Bunk, Boyke; Spröer, Cathrin; Neu, Thomas R.; Kuhlicke, Ute; Schmidt‐Hohagen, Kerstin; Hiller, Karsten; Bharat, Tanmay A. M.; Rachel, Reinhard; Spang, Anja; Gescher, Johannes

doi:10.1038/s41467-022-29263-y

“…Indeed, biofilm formation has been documented for multiple metabolically different archaeal species inhabiting highly diverse ecological niches (24, 25). Archaeal biofilms are thought to provide protection against various environmental stresses (26-28), promote horizontal gene exchange (29, 30) and enable syntrophy with other archaea and bacteria (31-34). Molecular studies on archaeal biofilm formation are still in their infancy and have largely focused on genetically tractable hyperthermophilic members of the order Sulfolobales and hyperhalophilic archaea of the class Halobacteria (24).…”

Section: Introductionmentioning

confidence: 99%

Archaeal bundling pili of Pyrobaculum calidifontis reveal similarities between archaeal and bacterial biofilms

Wang

¹

,

Cvirkaitė-Krupovič

²

,

Krupovìč

³

2022

Preprint

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While biofilms formed by bacteria have received great attention due to their importance in pathogenesis, much less research has been focused on the biofilms formed by archaea. It has been known that extracellular filaments in archaea, such as Type IV pili, hami and cannulae, play a part in the formation of archaeal biofilms. We have used cryo-electron microscopy to determine the atomic structure of a previously uncharacterized class of archaeal surface filaments from hyperthermophilic Pyrobaculum calidifontis. These filaments, which we call archaeal bundling pili (ABP), assemble into highly ordered bipolar bundles. The bipolar nature of these bundles most likely arises from the association of filaments from at least two different cells. The component protein shows homology, both at the sequence and structural level, to the bacterial protein TasA, a major component of the extracellular matrix in bacterial biofilms, contributing to biofilm stability. We show that ABP forms very stable filaments in a manner similar to the donor-strand exchange of bacterial TasA fibers and chaperone-usher pathway pili where a β-strand from one subunit is incorporated into a β-sheet of the next subunit. Our results reveal mechanistic similarities and evolutionary connection between bacterial and archaeal biofilms, and suggest that there could be many other archaeal surface filaments that are as yet uncharacterized.SignificanceBiofilms are communities of microbes where cells attach to each other as well as to surfaces, and bacterial biofilms have been intensively studied due to their importance in many infections. Much less has been known about archaeal biofilms, where archaea are a third domain of life. Using cryo-electron microscopy, we have determined the atomic structure of a surface filament in archaea that forms bi-polar bundles connecting cells. We show that this protein has common ancestry with a protein known to be an important component of bacterial biofilms. This adds to our understanding of the evolutionary relationship between bacteria and archaea and may provide new insights into bacterial biofilms.

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“…enable syntrophy with other archaea and bacteria (31)(32)(33)(34). Molecular studies on archaeal biofilm formation are still in their infancy and have largely focused on genetically tractable hyperthermophilic members of the order Sulfolobales and hyperhalophilic archaea of the class Halobacteria (24).…”

Section: Significancementioning

confidence: 99%

“…Indeed, biofilm formation has been documented for multiple metabolically different archaeal species inhabiting highly diverse ecological niches ( 24 , 25 ). Archaeal biofilms are thought to provide protection against various environmental stresses ( 26 – 28 ), promote horizontal gene exchange ( 29 , 30 ) and enable syntrophy with other archaea and bacteria ( 31 – 34 ). Molecular studies on archaeal biofilm formation are still in their infancy and have largely focused on genetically tractable hyperthermophilic members of the order Sulfolobales and hyperhalophilic archaea of the class Halobacteria ( 24 ).…”

mentioning

confidence: 99%

Archaeal bundling pili of Pyrobaculum calidifontis reveal similarities between archaeal and bacterial biofilms

Wang

¹

,

Cvirkaitė-Krupovič

²

,

Krupovìč

³

2022

Proc. Natl. Acad. Sci. U.S.A.

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While biofilms formed by bacteria have received great attention due to their importance in pathogenesis, much less research has been focused on the biofilms formed by archaea. It has been known that extracellular filaments in archaea, such as type IV pili, hami, and cannulae, play a part in the formation of archaeal biofilms. We have used cryo-electron microscopy to determine the atomic structure of a previously uncharacterized class of archaeal surface filaments from hyperthermophilic Pyrobaculum calidifontis. These filaments, which we call archaeal bundling pili (ABP), assemble into highly ordered bipolar bundles. The bipolar nature of these bundles most likely arises from the association of filaments from at least two different cells. The component protein, AbpA, shows homology, both at the sequence and structural level, to the bacterial protein TasA, a major component of the extracellular matrix in bacterial biofilms, contributing to biofilm stability. We show that AbpA forms very stable filaments in a manner similar to the donor-strand exchange of bacterial TasA fibers and chaperone-usher pathway pili where a β-strand from one subunit is incorporated into a β-sheet of the next subunit. Our results reveal likely mechanistic similarities and evolutionary connection between bacterial and archaeal biofilms, and suggest that there could be many other archaeal surface filaments that are as yet uncharacterized.

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“…The ectoparasitic interactions between Ignicoccus hospitalis and Nanoarchaeum equitans (the best characterised DPANN-host system) appears to involve membrane fusion between N. equitans and I. hospitalis generating a channel that connects the cytoplasms of both organisms 23 . ‘Cytoplasmic bridges’ have been observed between other DPANN and their hosts, and are thought to function in nutrient transfer 8, 24, 25 . However, the proteins forming or catalysing the formation of these structures are unknown 25 .…”

Section: Introductionmentioning

confidence: 99%

“…‘Cytoplasmic bridges’ have been observed between other DPANN and their hosts, and are thought to function in nutrient transfer 8, 24, 25 . However, the proteins forming or catalysing the formation of these structures are unknown 25 . Moreover, many DPANN appear to engage in interactions without forming such structures 21, 22, 26 , and the mechanism by which they acquire nutrients is unclear.…”

Section: Introductionmentioning

confidence: 99%

The parasitic lifestyle of an archaeal symbiont

Hamm

¹

,

Liao

²

,

Kügelgen

³

et al. 2023

Preprint

Self Cite

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DPANN Archaea are a diverse archaeal clade characterised by small cells and reduced genomes. To date, all cultivated DPANN Archaea are ectosymbionts that require direct cell cell interactions with a host archaeal species for proliferation. However, the dynamics of DPANN host interactions and the impacts of these interactions on host species are poorly understood. We show that the lifestyle of one DPANN archaeon (Candidatus Nanohaloarchaeum antarcticus) involves a cycle of attachment to host cells, invasion of the host cell cytoplasm, and subsequent lysis of the host cell. This is the first reported instance of such a predatory lifestyle amongst Archaea and indicates DPANN Archaea may be important players in microbial food webs across the biosphere. The internalisation of a symbiont cell within an archaeal host cell in the absence of phagocytotic machinery is relevant for models on the origin of the eukaryotic cell.

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

Cited by 21 publications

References 83 publications

Archaeal bundling pili of Pyrobaculum calidifontis reveal similarities between archaeal and bacterial biofilms

Archaeal bundling pili of Pyrobaculum calidifontis reveal similarities between archaeal and bacterial biofilms

Archaeal bundling pili of Pyrobaculum calidifontis reveal similarities between archaeal and bacterial biofilms

The parasitic lifestyle of an archaeal symbiont

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