S-layers at second glance? Altiarchaeal grappling hooks (hami) resemble archaeal S-layer proteins in structure and sequence.

Alexandra K Perras,Simonetta Gribaldo,Maximilian Mora,Musahid Ahmed,Lynelle K Takahashi,Alexander J Probst,Christine Moissl-Eichinger,Gerhard Wanner,Gerd Leitinger,Dagmar Kolb-Lenz,Annett Bellack,Andreas Klingl,Christine Ziegler,Bertram Daum,Anna Auerbach

doi:10.3389/fmicb.2015.00543

Abstract

The uncultivated “Candidatus Altiarchaeum hamiconexum” (formerly known as SM1 Euryarchaeon) carries highly specialized nano-grappling hooks (“hami”) on its cell surface. Until now little is known about the major protein forming these structured fibrous cell surface appendages, the genes involved or membrane anchoring of these filaments. These aspects were analyzed in depth in this study using environmental transcriptomics combined with imaging methods. Since a laboratory culture of this archaeon is not yet available, natural biofilm samples with high Ca. A. hamiconexum abundance were used for the entire analyses. The filamentous surface appendages spanned both membranes of the cell, which are composed of glycosyl-archaeol. The hami consisted of multiple copies of the same protein, the corresponding gene of which was identified via metagenome-mapped transcriptome analysis. The hamus subunit proteins, which are likely to self-assemble due to their predicted beta sheet topology, revealed no similiarity to known microbial flagella-, archaella-, fimbriae- or pili-proteins, but a high similarity to known S-layer proteins of the archaeal domain at their N-terminal region (44–47% identity). Our results provide new insights into the structure of the unique hami and their major protein and indicate their divergent evolution with S-layer proteins.

Highlights

In the course of evolution, nature has developed simple and fascinating solutions for various challenges
A. hamiconexum (Probst et al, 2014) are composed of one major protein species. The sequence of this hamus subunit protein did not show any homologies to currently known proteins involved in microbial fiber, pili, flagella, or archaella formation, but showed similarities to known archaeal surface layer proteins (S-layer) proteins: Besides a typical S-layer N-terminus pattern, the hamus subunit protein was found to be slightly acidic and most likely highly glycosylated, similar to S-layer proteins from e.g., Acidianus ambivalens and Metallosphaera sedula (Veith et al, 2009)
Previous modeling of beta-rich structures has shown that conformational diversity over a large number of repeats can lead to significantly different self-assemblies therein and that their final structure is determined by the way inherent flexibility is maintained via beta-sheet twists and bends (Makabe et al, 2006)

Summary

Introduction

In the course of evolution, nature has developed simple and fascinating solutions for various challenges. The sequence information retrieved can be used for assembly of near complete to complete genomes from key or underrepresented members of the communities (Tyson et al, 2004; Sharon and Banfield, 2013; Sharon et al, 2013). This information provides the basis for functional annotation of these novel microbial genomes. Linking metagenomic data from uncultivated microorganisms with information retrieved by other molecular methods and/or imaging techniques in order to characterize such unknown predicted proteins is a promising approach. Populations with low and simple diversity and uneven abundance of its members, such as the uncultivated acid mine drainage microbial community, can be studied in detail using a variety of these techniques, enabling researchers to link metagenomics to cellular characteristics (Comolli et al, 2009; Baker et al, 2010; Yelton et al, 2013; Comolli and Banfield, 2014)

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Conclusion