EMI_2751_sm_TableS5

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Table S5: Putative functions of genes of the large alginolyic operon of Z. galactanivorans
Gene ID
Zg2616
Zg2617
Putative function
Cation transporter
(NRAMP)
Sugar permease
Transcription regulator
Zg2620
Uptake of oligosaccharides
susD (B. thetaiotaomicron)
Zg2621
Uptake of oligosaccharides
susC (B. thetaiotaomicron)
Zg2623
unknown
kdgF (D. dadantii)
Zg2612
Homologue
Reference
mntH (E.coli)
Kehres et al, 2000
exuT (E. coli)
gntR (E. coli)
Nemoz et al, 1976
Izu et al., 1997
Anderson and Salyers,
1989b; Koropatlin et al,
2008
Anderson and Salyers,
1989b
Condemine and RobertBaudouy, 1991;
Hugouvieux-Cotte-Pattat
et al., 1996
Due to their position within the large alginolytic operon and to the fact that alginate induces
their transcription, we can confidently predict that the following genes also participate in
alginate assimilation in Zobellia galactanivorans. Thus, the SusCD-like outer membrane
proteins Zg2620 and Zg2621 are likely responsible for the uptake of alginate-oligosaccharides
from the extracellular medium to the periplasm, a role similar to the homologous system
characterized for starch utilization in Bacteroides thetaiotaomicron (Anderson and Salyers,
1989a, b; Koropatkin et al., 2008). The sugar permease Zg2616 is homologous to exuT which
is a Major Facilitator protein responsible of the uptake of aldohexuronate in Escherichia coli
(Nemoz et al., 1976). Therefore, Zg2616 probably transports alginate oligo- or
monosaccharides from the periplasm to the cytoplasm. The protein Zg2617 is homologous to
the transcription factor GntR which negatively regulates the gntRKU operon involved in the
uptake and catabolism of gluconate in E. coli (Izu et al., 1997). Whereas most of the ARgenes had low expression values in cells growing in the glucose-supplemented medium
(Table S3), zg2617 was already significantly transcribed. The transcription level of this gene
further increased 4-times when cells were grown in the alginate-containing medium. This
suggests that the protein Zg2617 acts as a transcription factor positively regulating the
alginolytic pathway in Z. galactanivorans. Such transcription activators are already known in
the GntR family (Neelakanta et al., 2009). Zg2623 is homologous to KdgF, a protein essential
to the pectinolytic system of Dickeya dadantii (Condemine and Robert-Baudouy, 1991;
Hugouvieux-Cotte-Pattat et al., 1996). Although the exact function of kdgF and zg2623 is
unknown, it is noteworthy that these genes are both conserved in operons dedicated to the
degradation of carboxylic polysaccharides (pectins and alginates) which play analogous roles
in the cell walls of plants and brown algae, respectively (Popper et al., 2011). Concomitant
with the induction of the catabolic pathway, the presence of alginate strongly increased the
expression of a putative cation transporter from the NRAMP family (Zg2612). The emergence
of such transporters was previously proposed as an adaptation to oxidative environments,
including those arising during infection of animals and plants (Kehres et al., 2000; Cellier et
al., 2001). Interestingly, brown algae defend themselves against pathogen aggressions by
transiently emitting reactive oxygen species which can notably control the growth of
epiphytic bacteria (Cosse et al., 2007). The protein Zg2612 might be part of a protection
mechanism towards this oxidative burst when Z. galactanivorans is degrading an algal cell
wall.
References
Anderson, K.L., and Salyers, A.A. (1989a) Genetic evidence that outer membrane binding of starch is
required for starch utilization by Bacteroides thetaiotaomicron. J Bacteriol 171: 3199-3204.
Anderson, K.L., and Salyers, A.A. (1989b) Biochemical evidence that starch breakdown by
Bacteroides thetaiotaomicron involves outer membrane starch-binding sites and periplasmic
starch-degrading enzymes. J Bacteriol 171: 3192-3198.
Cellier, M.F., Bergevin, I., Boyer, E., and Richer, E. (2001) Polyphyletic origins of bacterial Nramp
transporters. Trends Genet 17: 365-370.
Condemine, G., and Robert-Baudouy, J. (1991) Analysis of an Erwinia chrysanthemi gene cluster
involved in pectin degradation. Mol Microbiol 5: 2191-2202.
Cosse, A., Leblanc, C., and Potin, P. (2007) Dynamic defense of marine macroalgae against
pathogens: from early activated to gene-regulated responses. Adv Bot Res 46: 221-266.
Hugouvieux-Cotte-Pattat, N., Condemine, G., Nasser, W., and Reverchon, S. (1996) Regulation of
pectinolysis in Erwinia chrysanthemi. Annu Rev Microbiol 50: 213-257.
Izu, H., Adachi, O., and Yamada, M. (1997) Gene organization and transcriptional regulation of the
gntRKU operon involved in gluconate uptake and catabolism of Escherichia coli. J Mol Biol
267: 778-793.
Kehres, D.G., Zaharik, M.L., Finlay, B.B., and Maguire, M.E. (2000) The NRAMP proteins of
Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in
the response to reactive oxygen. Mol Microbiol 36: 1085-1100.
Koropatkin, N.M., Martens, E.C., Gordon, J.I., and Smith, T.J. (2008) Starch catabolism by a
prominent human gut symbiont is directed by the recognition of amylose helices. Structure 16:
1105-1115.
Neelakanta, G., Sankar, T.S., and Schnetz, K. (2009) Characterization of a beta-glucoside operon
(bgc) prevalent in septicemic and uropathogenic Escherichia coli strains. Appl Environ
Microbiol 75: 2284-2293.
Nemoz, G., Robert-Baudouy, J., and Stoeber, F. (1976) Physiological and genetic regulation of the
aldohexuronate transport system in Escherichia coli. J Bacteriol 127: 706-718.
Popper, Z.A., Michel, G., Herve, C., Domozych, D.S., Willats, W.G., Tuohy, M.G. et al. (2011)
Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol
62: 567-590.
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