Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides

Algal polysaccharides are an important bacterial nutrient source and central component of marine food webs. However, cellular and ecological aspects concerning the bacterial degradation of polysaccharide mixtures, as presumably abundant in natural habitats, are poorly understood. Here, we contextual...

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Veröffentlicht in:The ISME Journal 2019-01, Vol.13 (1), p.92-103
Hauptverfasser: Koch, Hanna, Dürwald, Alexandra, Schweder, Thomas, Noriega-Ortega, Beatriz, Vidal-Melgosa, Silvia, Hehemann, Jan-Hendrik, Dittmar, Thorsten, Freese, Heike M., Becher, Dörte, Simon, Meinhard, Wietz, Matthias
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container_issue 1
container_start_page 92
container_title The ISME Journal
container_volume 13
creator Koch, Hanna
Dürwald, Alexandra
Schweder, Thomas
Noriega-Ortega, Beatriz
Vidal-Melgosa, Silvia
Hehemann, Jan-Hendrik
Dittmar, Thorsten
Freese, Heike M.
Becher, Dörte
Simon, Meinhard
Wietz, Matthias
description Algal polysaccharides are an important bacterial nutrient source and central component of marine food webs. However, cellular and ecological aspects concerning the bacterial degradation of polysaccharide mixtures, as presumably abundant in natural habitats, are poorly understood. Here, we contextualize marine polysaccharide mixtures and their bacterial utilization in several ways using the model bacterium Alteromonas macleodii 83-1, which can degrade multiple algal polysaccharides and contributes to polysaccharide degradation in the oceans. Transcriptomic, proteomic and exometabolomic profiling revealed cellular adaptations of A. macleodii 83-1 when degrading a mix of laminarin, alginate and pectin. Strain 83-1 exhibited substrate prioritization driven by catabolite repression, with initial laminarin utilization followed by simultaneous alginate/pectin utilization. This biphasic phenotype coincided with pronounced shifts in gene expression, protein abundance and metabolite secretion, mainly involving CAZymes/polysaccharide utilization loci but also other functional traits. Distinct temporal changes in exometabolome composition, including the alginate/pectin-specific secretion of pyrroloquinoline quinone, suggest that substrate-dependent adaptations influence chemical interactions within the community. The ecological relevance of cellular adaptations was underlined by molecular evidence that common marine macroalgae, in particular Saccharina and Fucus , release mixtures of alginate and pectin-like rhamnogalacturonan. Moreover, CAZyme microdiversity and the genomic predisposition towards polysaccharide mixtures among Alteromonas spp. suggest polysaccharide-related traits as an ecophysiological factor, potentially relating to distinct ‘carbohydrate utilization types’ with different ecological strategies. Considering the substantial primary productivity of algae on global scales, these insights contribute to the understanding of bacteria–algae interactions and the remineralization of chemically diverse polysaccharide pools, a key step in marine carbon cycling.
doi_str_mv 10.1038/s41396-018-0252-4
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However, cellular and ecological aspects concerning the bacterial degradation of polysaccharide mixtures, as presumably abundant in natural habitats, are poorly understood. Here, we contextualize marine polysaccharide mixtures and their bacterial utilization in several ways using the model bacterium Alteromonas macleodii 83-1, which can degrade multiple algal polysaccharides and contributes to polysaccharide degradation in the oceans. Transcriptomic, proteomic and exometabolomic profiling revealed cellular adaptations of A. macleodii 83-1 when degrading a mix of laminarin, alginate and pectin. Strain 83-1 exhibited substrate prioritization driven by catabolite repression, with initial laminarin utilization followed by simultaneous alginate/pectin utilization. This biphasic phenotype coincided with pronounced shifts in gene expression, protein abundance and metabolite secretion, mainly involving CAZymes/polysaccharide utilization loci but also other functional traits. 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subjects 38/91
45/77
631/326/171/1878
631/337/2019
82/16
82/58
Abundance
Acclimatization
Adaptation
Adaptation, Physiological
Algae
Alginates
Alginates - metabolism
Alginic acid
Alteromonas - genetics
Alteromonas - physiology
Alteromonas macleodii
Bacteria
Biodegradation
Biomedical and Life Sciences
Carbohydrates
Carbon cycle
Catabolite repression
Chemical interactions
Degradation
Ecological effects
Ecology
Ecosystem
Evolutionary Biology
Food chains
Food webs
Gene expression
Laminarin
Life Sciences
Metabolites
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Oceans
Organic chemistry
Pectin
Phenotypes
Polysaccharides
Polysaccharides - metabolism
Proteins
Proteomics
Pyrroloquinoline quinone
Quinones
Remineralization
Rhamnogalacturonan
Saccharides
Seaweeds
Secretion
Substrates
Utilization
title Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides
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