Transport capabilities of eleven gram-positive bacteria: Comparative genomic analyses

Lorca, Graciela L., Barabote, Ravi D., Zlotopolski, Vladimir, Tran, Can, Winnen, Brit, Hvorup, Rikki N., Stonestrom, Aaron J., Nguyen, Elizabeth, Huang, Li-Wen, Kim, David S. and Saier Jr., Milton H. (2007) Transport capabilities of eleven gram-positive bacteria: Comparative genomic analyses. BBA: Biomembranes, 1768 6: 1342-1366. doi:10.1016/j.bbamem.2007.02.007

Author Lorca, Graciela L.
Barabote, Ravi D.
Zlotopolski, Vladimir
Tran, Can
Winnen, Brit
Hvorup, Rikki N.
Stonestrom, Aaron J.
Nguyen, Elizabeth
Huang, Li-Wen
Kim, David S.
Saier Jr., Milton H.
Title Transport capabilities of eleven gram-positive bacteria: Comparative genomic analyses
Journal name BBA: Biomembranes   Check publisher's open access policy
ISSN 0005-2736
Publication date 2007-06-01
Sub-type Article (original research)
DOI 10.1016/j.bbamem.2007.02.007
Open Access Status DOI
Volume 1768
Issue 6
Start page 1342
End page 1366
Total pages 25
Editor J-M. Ruysschaert
R. M. Epand
Place of publication Amsterdam, Netherlands
Publisher Elsevier
Language eng
Subject 0601 Biochemistry and Cell Biology
0904 Chemical Engineering
Abstract Type IV pili (Tfp), which have been studied extensively in a few Gram-negative species, are the paradigm of a group of widespread and functionally versatile nano-machines. Here, we performed the most detailed molecular characterisation of Tfp in a Gram-positive bacterium. We demonstrate that the naturally competent Streptococcus sanguinis produces retractable Tfp, which like their Gram-negative counterparts can generate hundreds of piconewton of tensile force and promote intense surface-associated motility. Tfp power 'train-like' directional motion parallel to the long axis of chains of cells, leading to spreading zones around bacteria grown on plates. However, S. sanguinis Tfp are not involved in DNA uptake, which is mediated by a related but distinct nano-machine, and are unusual because they are composed of two pilins in comparable amounts, rather than one as normally seen. Whole genome sequencing identified a locus encoding all the genes involved in Tfp biology in S. sanguinis. A systematic mutational analysis revealed that Tfp biogenesis in S. sanguinis relies on a more basic machinery (only 10 components) than in Gram-negative species and that a small subset of four proteins dispensable for pilus biogenesis are essential for motility. Intriguingly, one of the piliated mutants that does not exhibit spreading retains microscopic motility but moves sideways, which suggests that the corresponding protein controls motion directionality. Besides establishing S. sanguinis as a useful new model for studying Tfp biology, these findings have important implications for our understanding of these widespread filamentous nano-machines.
Formatted abstract
The genomes of eleven Gram-positive bacteria that are important for human health and the food industry, nine low G+C lactic acid bacteria and two high G+C Gram-positive organisms, were analyzed for their complement of genes encoding transport proteins. Thirteen to 18% of their genes encode transport proteins, larger percentages than observed for most other bacteria. All of these bacteria possess channel proteins, some of which probably function to relieve osmotic stress. Amino acid uptake systems predominate over sugar and peptide cation symporters, and of the sugar uptake porters, those specific for oligosaccharides and glycosides often outnumber those for free sugars, About 10% of the total transport proteins are constituents of putative multidrug efflux pumps with Major Facilitator Superfamily (MFS)-type pumps (55%) being more prevalent than ATP-binding cassette (ABC)-type pumps (33%), which, however, usually greatly outnumber all other types. An exception to this generalization is Streptococcus thermophilus with 54% of its drug efflux pumps belonging to the ABC superfamily and 23% belonging each to the Multidrug/Oligosaccharide/Polysaccharide (MOP) superfamily and the MFS. These bacteria also display peptide efflux pumps that may function in intercellular signalling, and macromolecular efflux pumps, many of predictable specificities. Most of the bacteria analyzed have no pmf-coupled or transmembrane flow electron carriers. The one exception is Brevibacterium linens, which in addition to these carriers, also has transporters of several families not represented in the other ten bacteria examined. Comparisons with the genomes of organisms from other bacterial kingdoms revealed that lactic acid bacteria possess distinctive proportions of recognized transporter types (e.g., more porters specific for glycosides than reducing sugars). Some homologues of transporters identified had previously been identified only in Gram-negative bacteria or in eukaryotes. Our studies reveal unique characteristics of the lactic acid bacteria such as the universal presence of genes encoding mechanosensitive channels, competence systems and large numbers of sugar transporters of the phosphotransferase system. The analyses lead to important physiological predictions regarding the preferred signalling and metabolic activities of these industrially important bacteria.
© 2007 Elsevier B.V. All rights reserved.
Keyword Lactic acid bacteria
Transport proteins
Genomic analyses
Q-Index Code C1
Grant ID MR/J006874/1
SC2 AI116566
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Excellence in Research Australia (ERA) - Collection
Institute for Molecular Bioscience - Publications
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Citation counts: TR Web of Science Citation Count  Cited 51 times in Thomson Reuters Web of Science Article | Citations
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Created: Thu, 18 Feb 2010, 21:12:59 EST by Sue Green on behalf of Institute for Molecular Bioscience