In vitro assembly of the bacterial actin protein MamK from ' Candidatus Magnetobacterium casensis' in the phylum Nitrospirae.

Aihua Deng,Hua Bai,Wei Lin,Zhaopeng Sun,Yongxin Pan,Jie Wu,Qinyun Sun,Tingyi Wen,Nana Shi

doi:10.1007/s13238-016-0253-x

Abstract

Magnetotactic bacteria (MTB), a group of phylogenetically diverse organisms that use their unique intracellular magnetosome organelles to swim along the Earth’s magnetic field, play important roles in the biogeochemical cycles of iron and sulfur. Previous studies have revealed that the bacterial actin protein MamK plays essential roles in the linear arrangement of magnetosomes in MTB cells belonging to the Proteobacteria phylum. However, the molecular mechanisms of multiple-magnetosome-chain arrangements in MTB remain largely unknown. Here, we report that the MamK filaments from the uncultivated ‘Candidatus Magnetobacterium casensis’ (Mcas) within the phylum Nitrospirae polymerized in the presence of ATP alone and were stable without obvious ATP hydrolysis-mediated disassembly. MamK in Mcas can convert NTP to NDP and NDP to NMP, showing the highest preference to ATP. Unlike its Magnetospirillum counterparts, which form a single magnetosome chain, or other bacterial actins such as MreB and ParM, the polymerized MamK from Mcas is independent of metal ions and nucleotides except for ATP, and is assembled into well-ordered filamentous bundles consisted of multiple filaments. Our results suggest a dynamically stable assembly of MamK from the uncultivated Nitrospirae MTB that synthesizes multiple magnetosome chains per cell. These findings further improve the current knowledge of biomineralization and organelle biogenesis in prokaryotic systems.Electronic supplementary materialThe online version of this article (doi:10.1007/s13238-016-0253-x) contains supplementary material, which is available to authorized users.

Highlights

Cytoskeletal proteins have been identified in all organisms as a basic structural framework
Previous studies have revealed that the bacterial actin protein MamK plays essential roles in the linear arrangement of magnetosomes in Magnetotactic bacteria (MTB) cells belonging to the Proteobacteria phylum
We report that the MamK filaments from the uncultivated ‘Candidatus Magnetobacterium casensis’ (Mcas) within the phylum Nitrospirae polymerized in the presence of ATP alone and were stable without obvious ATP hydrolysis-mediated disassembly

Summary

Introduction

Cytoskeletal proteins have been identified in all organisms as a basic structural framework They are critical for many important cellular processes, such as cell growth, shape maintenance, cell division, motility and internal transport pathways (Pollard and Cooper, 2009; Shih and Rothfield, 2006; Cabeen and Jacobs-Wagner, 2005, 2010). Approximately 40 different actin protein families sharing less than 30% identity have been discovered in prokaryotic organisms (Derman et al, 2009) Despite their low sequence identities, all bacterial actin proteins contain a similar tertiary structure and a common ATP-binding pocket (Carballido, 2006). MreB, ParM, FtsA and MamK form four phylogenetically and functionally distinct groups of bacterial actin proteins and play vital roles in controlling cell shape (Reimold et al, 2013), segregating plasmid DNA (Garner et al, 2004), dividing cells (Szwedziak et al, 2012) and organizing the subcellular magnetosome chain structure (Komeili et al, 2006), respectively (Fig. 1)

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