Polysaccharides from macroalgae are important bacterial nutrient source and central biogeochemical component in the oceans. To illuminate the cellular mechanisms of polysaccharide degradation by marine bacteria, growth of Alteromonas macleodii 83-1 on a mix of laminarin, alginate and pectin was characterized using transcriptomics, proteomics and exometabolomics. A. macleodii 83-1 showed two distinct growth stages, with exponential growth during laminarin utilization followed by maintenance during simultaneous alginate/pectin utilization. The biphasic growth coincided with major temporal shifts in gene expression and metabolite secretion, enabling to define major/accessory polysaccharide utilization loci, reconstruct the complete degradation pathways for each polysaccharide, as well as identify temporal phenotypes in other relevant traits. FT-ICR-MS revealed a distinct suite of secreted metabolites for each growth phase, with pyrroloquinoline quinone exclusively produced with alginate/pectin. The finding of substrate-unique phenotypes indicates an exquisite adaptation to polysaccharide utilization with probable relevance for the degradation of macroalgal biomass, which comprises a complex mix of polysaccharides. Moreover, substrate-unique exometabolomes possibly influence metabolic interactions with other community members. Overall, the presence of fine-tuned genetic machineries for polysaccharide degradation and the widespread detection of related CAZymes in global locations indicate an ecological relevance of A. macleodii in marine polysaccharide cycling and bacteria-algae interactions. Overall design: Alteromonas macleodii 83-1 cells were grown on a mix of three polysaccharides (laminarin, pectin, alginate) in triplicates (Mix1-3). As control, cells were grown on glucose also in triplicates (Glucose1-3). For both incubations, biomass samples were taken at two time points T1 (13h) and T2 (21h of incubation) and transcriptomics analyses were performed by doing RNA-Seq. Please note that the FASTA file contains the nucleotide sequences of all genes of the genome, which were used as a reference to obtain transcript abundance counts by aligning them onto the gene sequences. The genome sequence is deposited in the DOE JGI-IMG/MER database (accession number 2716884210).