<named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation

ABSTRACT The ability to form biofilms is shared by many microorganisms, including archaea. Cells in a biofilm are encased in extracellular polymeric substances that typically include polysaccharides, proteins, and extracellular DNA, conferring protection while providing a structure that allows for o...

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Autores principales:	Heather Schiller, Stefan Schulze, Zuha Mutan, Charlotte de Vaulx, Catalina Runcie, Jessica Schwartz, Theopi Rados, Alexandre W. Bisson Filho, Mechthild Pohlschroder
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Haloferax volcanii anaerobiosis archaea archaella bacterioruberins biofilms Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9db9012156f142748edb701ab095e065
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spelling	oai:doaj.org-article:9db9012156f142748edb701ab095e0652021-11-15T15:31:13Z<named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation10.1128/mSphere.00976-202379-5042https://doaj.org/article/9db9012156f142748edb701ab095e0652020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00976-20https://doaj.org/toc/2379-5042ABSTRACT The ability to form biofilms is shared by many microorganisms, including archaea. Cells in a biofilm are encased in extracellular polymeric substances that typically include polysaccharides, proteins, and extracellular DNA, conferring protection while providing a structure that allows for optimal nutrient flow. In many bacteria, flagella and evolutionarily conserved type IV pili are required for the formation of biofilms on solid surfaces or floating at the air-liquid interface of liquid media. Similarly, in many archaea it has been demonstrated that type IV pili and, in a subset of these species, archaella are required for biofilm formation on solid surfaces. Additionally, in the model archaeon Haloferax volcanii, chemotaxis and AglB-dependent glycosylation play important roles in this process. H. volcanii also forms immersed biofilms in liquid cultures poured into petri dishes. This study reveals that mutants of this haloarchaeon that interfere with the biosynthesis of type IV pili or archaella, as well as a chemotaxis-targeting transposon and aglB deletion mutants, lack obvious defects in biofilms formed in liquid cultures. Strikingly, we have observed that these liquid-based biofilms are capable of rearrangement into honeycomb-like patterns that rapidly form upon removal of the petri dish lid, a phenomenon that is not dependent on changes in light or oxygen concentration but can be induced by controlled reduction of humidity. Taken together, this study demonstrates that H. volcanii requires novel, unidentified strategies for immersed liquid biofilm formation and also exhibits rapid structural rearrangements. IMPORTANCE This first molecular biological study of archaeal immersed liquid biofilms advances our basic biological understanding of the model archaeon Haloferax volcanii. Data gleaned from this study also provide an invaluable foundation for future studies to uncover components required for immersed liquid biofilms in this haloarchaeon and also potentially for liquid biofilm formation in general, which is poorly understood compared to the formation of biofilms on surfaces. Moreover, this first description of rapid honeycomb pattern formation is likely to yield novel insights into the underlying structural architecture of extracellular polymeric substances and cells within immersed liquid biofilms.Heather SchillerStefan SchulzeZuha MutanCharlotte de VaulxCatalina RuncieJessica SchwartzTheopi RadosAlexandre W. Bisson FilhoMechthild PohlschroderAmerican Society for MicrobiologyarticleHaloferax volcaniianaerobiosisarchaeaarchaellabacterioruberinsbiofilmsMicrobiologyQR1-502ENmSphere, Vol 5, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Haloferax volcanii anaerobiosis archaea archaella bacterioruberins biofilms Microbiology QR1-502
spellingShingle	Haloferax volcanii anaerobiosis archaea archaella bacterioruberins biofilms Microbiology QR1-502 Heather Schiller Stefan Schulze Zuha Mutan Charlotte de Vaulx Catalina Runcie Jessica Schwartz Theopi Rados Alexandre W. Bisson Filho Mechthild Pohlschroder <named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation
description	ABSTRACT The ability to form biofilms is shared by many microorganisms, including archaea. Cells in a biofilm are encased in extracellular polymeric substances that typically include polysaccharides, proteins, and extracellular DNA, conferring protection while providing a structure that allows for optimal nutrient flow. In many bacteria, flagella and evolutionarily conserved type IV pili are required for the formation of biofilms on solid surfaces or floating at the air-liquid interface of liquid media. Similarly, in many archaea it has been demonstrated that type IV pili and, in a subset of these species, archaella are required for biofilm formation on solid surfaces. Additionally, in the model archaeon Haloferax volcanii, chemotaxis and AglB-dependent glycosylation play important roles in this process. H. volcanii also forms immersed biofilms in liquid cultures poured into petri dishes. This study reveals that mutants of this haloarchaeon that interfere with the biosynthesis of type IV pili or archaella, as well as a chemotaxis-targeting transposon and aglB deletion mutants, lack obvious defects in biofilms formed in liquid cultures. Strikingly, we have observed that these liquid-based biofilms are capable of rearrangement into honeycomb-like patterns that rapidly form upon removal of the petri dish lid, a phenomenon that is not dependent on changes in light or oxygen concentration but can be induced by controlled reduction of humidity. Taken together, this study demonstrates that H. volcanii requires novel, unidentified strategies for immersed liquid biofilm formation and also exhibits rapid structural rearrangements. IMPORTANCE This first molecular biological study of archaeal immersed liquid biofilms advances our basic biological understanding of the model archaeon Haloferax volcanii. Data gleaned from this study also provide an invaluable foundation for future studies to uncover components required for immersed liquid biofilms in this haloarchaeon and also potentially for liquid biofilm formation in general, which is poorly understood compared to the formation of biofilms on surfaces. Moreover, this first description of rapid honeycomb pattern formation is likely to yield novel insights into the underlying structural architecture of extracellular polymeric substances and cells within immersed liquid biofilms.
format	article
author	Heather Schiller Stefan Schulze Zuha Mutan Charlotte de Vaulx Catalina Runcie Jessica Schwartz Theopi Rados Alexandre W. Bisson Filho Mechthild Pohlschroder
author_facet	Heather Schiller Stefan Schulze Zuha Mutan Charlotte de Vaulx Catalina Runcie Jessica Schwartz Theopi Rados Alexandre W. Bisson Filho Mechthild Pohlschroder
author_sort	Heather Schiller
title	<named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation
title_short	<named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation
title_full	<named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation
title_fullStr	<named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation
title_full_unstemmed	<named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation
title_sort	<named-content content-type="genus-species">haloferax volcanii</named-content> immersed liquid biofilms develop independently of known biofilm machineries and exhibit rapid honeycomb pattern formation
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/9db9012156f142748edb701ab095e065
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<named-content content-type="genus-species">Haloferax volcanii</named-content> Immersed Liquid Biofilms Develop Independently of Known Biofilm Machineries and Exhibit Rapid Honeycomb Pattern Formation

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