Different utilization of alginate and other algal polysaccharides by marine Alteromonas macleodii ecotypes

Summary The marine bacterium Alteromonas macleodii is a copiotrophic r‐strategist, but little is known about its potential to degrade polysaccharides. Here, we studied the degradation of alginate and other algal polysaccharides by A. macleodii strain 83‐1 in comparison to other A. macleodii strains....

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Published inEnvironmental microbiology Vol. 17; no. 10; pp. 3857 - 3868
Main Authors Neumann, Anna M., Balmonte, John P., Berger, Martine, Giebel, Helge-Ansgar, Arnosti, Carol, Voget, Sonja, Simon, Meinhard, Brinkhoff, Thorsten, Wietz, Matthias
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.10.2015
Wiley Subscription Services, Inc
Subjects
Algae
Alginates - metabolism
Alteromonas - genetics
Alteromonas - isolation & purification
Alteromonas - metabolism
Alteromonas macleodii
Aquatic Organisms - genetics
Aquatic Organisms - metabolism
Atlantic Ocean
Bacterial Proteins - genetics
Bacteriology
Ecotype
Energy Metabolism - physiology
Genome, Bacterial - genetics
Genomes
Genomic Islands - genetics
Glucans - metabolism
Glucuronic Acid - metabolism
Hexuronic Acids - metabolism
Membrane Proteins - genetics
Metagenome - genetics
Polysaccharide-Lyases - genetics
Polysaccharide-Lyases - metabolism
Seawater - microbiology
Xylans - metabolism
Atlantic Ocean
A, Atlantic
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Summary:Summary The marine bacterium Alteromonas macleodii is a copiotrophic r‐strategist, but little is known about its potential to degrade polysaccharides. Here, we studied the degradation of alginate and other algal polysaccharides by A. macleodii strain 83‐1 in comparison to other A. macleodii strains. Cell densities of strain 83‐1 with alginate as sole carbon source were comparable to those with glucose, but the exponential phase was delayed. The genome of 83‐1 was found to harbour an alginolytic system comprising five alginate lyases, whose expression was induced by alginate. The alginolytic system contains additional CAZymes, including two TonB‐dependent receptors, and is part of a 24 kb genomic island unique to the A. macleodii ‘surface clade’ ecotype. In contrast, strains of the ‘deep clade’ ecotype contain only a single alginate lyase in a separate 7 kb island. This difference was reflected in an eightfold greater efficiency of surface clade strains to grow on alginate. Strain 83‐1 furthermore hydrolysed laminarin, pullulan and xylan, and corresponding polysaccharide utilization loci were detected in the genome. Alteromonas macleodii alginate lyases were predominantly detected in Atlantic Ocean metagenomes. The demonstrated hydrolytic capacities are likely of ecological relevance and represent another level of adaptation among A. macleodii ecotypes.
Bibliography:U.S. National Science Foundation - No. OCE-1332881
ark:/67375/WNG-FMBH8RBZ-3
German Research Foundation (DFG) - No. WI3888/1-1; No. TRR 51
ArticleID:EMI12862
istex:F12DE1D5246DAD4A82B2A6DBC293F0BA02DDB763
Fig. S1. Maximum likelihood phylogeny of 12 Alteromonas macleodii strains based on a 2.3 Mb alignment of 2340 single-copy core genes, confirming the affiliation of strain 83-1 with the A. macleodii surface clade. Circles indicate nodes with > 95% bootstrap support in 1000 replicates. Fig. S2. Comparison of alginolytic systems (AS) in Alteromonas macleodii strain 83-1, other Alteromonadales, as well as the flavobacteria Gramella forsetii and Formosa agariphila. Gene designations in strain 83-1 correspond to IMG locus tags shown in Table S2. As indicated by the gray box and gray-shaded genes, Pseudoalteromonas haloplanktis, Pseudoalteromonas marina and Shewanella waksmanii all contain the 'AS core' consisting of alginate lyases PL6 and PL17 and adjacent cupin-domain, sugar permease, sugar kinase and isobutyrate dehydrogenase genes (Table S2). Fig. S3. (A) Alginolytic system in genomic island specific to the Alteromonas macleodii deep clade. Alginolytic system containing a PL6 alginate lyase, three other CAZymes (1: putative 4-hydroxy-2-oxoglutarate aldolase; 2/3: putative ketodeoxygluconokinases), a putative diguanylate cyclase (DGC), a hypothetical protein (HP), as well as a GntR-family transcriptional regulator (GntR). (B) Growth of surface versus deep clade strains with alginate. The presence of only a single alginate lyase in comparison to five lyases in surface clade strains (Fig. 2) was reflected in substantially lower alginolytic capacities, as illustrated by an eightfold lower cell density of deep clade strain U7 in comparison to strain 83-1 after cultivation for 48 h with alginate as sole carbon source. Fig. S4. Growth of Alteromonas macleodii strain 83-1 with an exudate of Synechococcus sp. RCC2527 (solid line) in comparison to sterile f/2 medium as negative control (dotted line). Table S1. Origin and genome characteristics of Alteromonas macleodii strains analysed in the present study. Table S2. Alginolytic system in Alteromonas macleodii strain 83-1 and homologous genes in Zobellia galactanivorans DsijT (Thomas et al., 2012). Table S3. Polysaccharide utilization loci (PUL) in Alteromonas macleodii strain 83-1 associated with the degradation of xylan, laminarin and pullulan. Table S4. Metagenomes in the Integrated Microbial Metagenome (IMG/M) database searched for alginate lyases from Alteromonas macleodii. Table S5. Primer and probes used for RT-qPCR of alginate lyases and the rpoB reference gene.
Hanse-Wissenschaftskolleg (Delmenhorst, Germany)
ObjectType-Article-1
SourceType-Scholarly Journals-1
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content type line 23
ISSN:1462-2912
1462-2920
DOI:10.1111/1462-2920.12862