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TAT-Pathway-Dependent Lipoproteins as a Niche-Based Adaptation in Prokaryotes

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Abstract

Bacterial lipoproteins, characterized by the N-terminal N-acyl S-diacylglyceryl Cysteine, are key membrane proteins in bacterial homeostasis. It is generally thought that during the modification lipoprotein precursors are translocated via the Sec-machinery in an unfolded state. The recent discovery of twin-arginine translocation (TAT) machinery, meant for exporting folded-proteins, and the presence of TAT-type signal sequences in co-factor-containing (hence already folded) lipoproteins, prompted us to investigate its role and significance in lipoprotein biosynthesis. We systematically analyzed 696 prokaryotic genomes using an algorithm based on DOLOP and TatP rules to predict TAT-pathway-dependent lipoprotein substrates. Occurrence of the deduced TAT-pathway-dependent lipoprotein substrates in relation to genome size, presence or absence of TAT machinery, and extent of its usage for lipoprotein export and habitat types revealed that unlike the host-obligates, the free-living prokaryotes in complex hostile environments (e.g., soil) depend more on TAT-exported lipoproteins. Functional classification of the predicted TAT-dependent lipoproteins revealed enrichment in hydrolases and oxido-reductases, which are fast-folding and co-factor-containing proteins. The role of the TAT pathway in the export of folded-lipoproteins and in niche-specific adaptation for survival has important implications not only in lipoprotein biosynthesis, but also for protein and metabolic engineering applications.

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Acknowledgments

We thank A. Tamil Selvan for the algorithm and script. We are grateful to Prof. Edward J. Behrman, Ohio State University, USA for his critical inputs to improve the readability of the manuscript and Prof. Venkat Gopalan, Ohio State University, USA for his valuable help. UGC-DRS and DBT-Center of Excellence programmes are acknowledged for financial support and fellowship to HS. MMB acknowledges the Medical Research Council, UK, Darwin College Cambridge and Schlumberger Ltd. for support.

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Correspondence to Krishnan Sankaran.

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Shruthi, H., Madan Babu, M. & Sankaran, K. TAT-Pathway-Dependent Lipoproteins as a Niche-Based Adaptation in Prokaryotes. J Mol Evol 70, 359–370 (2010). https://doi.org/10.1007/s00239-010-9334-2

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