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Haloferax volcanii immersed liquid biofilms develop independently of known biofilm machineries and exhibit rapid honeycomb pattern formation

Heather Schiller, View ORCID ProfileStefan Schulze, Zuha Mutan, Charlotte de Vaulx, Catalina Runcie, Jessica Schwartz, Theopi Rados, View ORCID ProfileAlexandre W. Bisson Filho, View ORCID ProfileMechthild Pohlschroder
doi: https://doi.org/10.1101/2020.07.18.206797
Heather Schiller
1University of Pennsylvania, Department of Biology, Leidy Laboratories, Philadelphia, USA
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Stefan Schulze
1University of Pennsylvania, Department of Biology, Leidy Laboratories, Philadelphia, USA
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  • ORCID record for Stefan Schulze
Zuha Mutan
1University of Pennsylvania, Department of Biology, Leidy Laboratories, Philadelphia, USA
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Charlotte de Vaulx
1University of Pennsylvania, Department of Biology, Leidy Laboratories, Philadelphia, USA
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Catalina Runcie
1University of Pennsylvania, Department of Biology, Leidy Laboratories, Philadelphia, USA
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Jessica Schwartz
1University of Pennsylvania, Department of Biology, Leidy Laboratories, Philadelphia, USA
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Theopi Rados
2Department of Biology, Rosenstiel Basic Medical Science Research Center, Brandeis University, Waltham, Massachusetts, USA
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Alexandre W. Bisson Filho
2Department of Biology, Rosenstiel Basic Medical Science Research Center, Brandeis University, Waltham, Massachusetts, USA
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Mechthild Pohlschroder
1University of Pennsylvania, Department of Biology, Leidy Laboratories, Philadelphia, USA
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  • ORCID record for Mechthild Pohlschroder
  • For correspondence: pohlschr@sas.upenn.edu
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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. In the model archaeon Haloferax volcanii, chemotaxis and AglB-dependent glycosylation also play a role in this process. H. volcanii also forms immersed biofilms in liquid cultures poured into Petri dishes. This study reveals that mutants of this haloar-chaeon that interfere with the biosynthesis of type IV pili or archaella, as well as chemotaxis 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 and are not dependent on changes in light, oxygen, or humidity. Taken together, this study demonstrates that H. volcanii requires novel, as yet unidentified strategies for immersed liquid biofilm formation and also exhibits rapid structural rearrangements, providing the first evidence for a potential role for volatile signaling in H. volcanii.

Importance This first molecular biological study of archaeal immersed liquid biofilms advances our basic biology 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, the discovery of honeycomb pattern formation is likely to yield novel insights into the underlying interactions between the exopolysaccharide structure and cell arrangements within these biofilms and uncover mechanisms of cell-cell communication, a highly understudied topic in archaea.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 18, 2020.
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Haloferax volcanii immersed liquid biofilms develop independently of known biofilm machineries and exhibit rapid honeycomb pattern formation
Heather Schiller, Stefan Schulze, Zuha Mutan, Charlotte de Vaulx, Catalina Runcie, Jessica Schwartz, Theopi Rados, Alexandre W. Bisson Filho, Mechthild Pohlschroder
bioRxiv 2020.07.18.206797; doi: https://doi.org/10.1101/2020.07.18.206797
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Haloferax volcanii immersed liquid biofilms develop independently of known biofilm machineries and exhibit rapid honeycomb pattern formation
Heather Schiller, Stefan Schulze, Zuha Mutan, Charlotte de Vaulx, Catalina Runcie, Jessica Schwartz, Theopi Rados, Alexandre W. Bisson Filho, Mechthild Pohlschroder
bioRxiv 2020.07.18.206797; doi: https://doi.org/10.1101/2020.07.18.206797

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