Abstract
Polysaccharide particles are important substrates and microhabitats for marine bacteria. However, substrate-specific bacterial dynamics in mixtures of particle types with different polysaccharide composition, as likely occurring in natural habitats, are undescribed. Here, we studied the composition, functional diversity and gene expression of marine bacterial communities colonizing a mix of alginate and pectin particles. Amplicon, metagenome and metatranscriptome sequencing revealed that communities on alginate and pectin particles significantly differed from their free-living counterparts. Unexpectedly, microbial dynamics on alginate and pectin particles were similar, with predominance of amplicon sequence variants (ASVs) from Tenacibaculum, Colwellia, Psychrobium and Psychromonas. Corresponding metagenome-assembled genomes (MAGs) expressed diverse alginate lyases, several colocalized in polysaccharide utilization loci. Only a single, low-abundant MAG showed elevated transcript abundances of pectin-degrading enzymes. One specific Glaciecola ASV dominated the free-living fraction, possibly persisting on particle-derived oligomers through different glycoside hydrolases. Elevated ammonium uptake and metabolism signified nitrogen as an important factor for degrading carbon-rich particles, whereas elevated methylcitrate and glyoxylate cycles suggested nutrient limitation in surrounding waters. The bacterial preference for alginate, whereas pectin primarily served as colonization scaffold, illuminates substrate-driven dynamics within mixed polysaccharide pools. These insights expand our understanding of bacterial niche specialization and the biological carbon pump in macroalgae-rich habitats.
Highlights
SummaryPolysaccharide particles are important substrates and microhabitats for marine bacteria
The FL fraction was obtained by 5 μm filtration to remove non-magnetic particles and collecting the flow-through on 0.2 μm filters (Supplementary Fig. 1B)
We only detected three PL1 pectate lyases and few other pectin-related genes (CE8, GH28, GH105). These results indicate that pectin is not a prime bacterial substrate in kelp forests, pectinolytic bacteria occur in diverse marine habitats (Van Truong et al, 2001; Hehemann et al, 2017; Hobbs et al, 2019) and pectinous substrates are exuded by Helgoland macroalgae (Koch et al, 2019a)
Summary
Polysaccharide particles are important substrates and microhabitats for marine bacteria. The chemical and structural complexity of marine hydrogels challenges the identification of specific particle–microbe relationships To reduce this complexity, exposing synthetic model particles to natural bacterioplankton helps understanding the dynamics and drivers of particle colonization. CAZyme numbers, diversity and genomic organization can distinguish bacteria in primary degraders for initial polymer breakdown, and secondary consumers utilizing oligosaccharides, monosaccharides or other compounds released by primary degraders These types occur across taxonomic boundaries and within single species (Hehemann et al, 2016; Koch et al, 2020). The co-availability of hydrogels with different polysaccharide composition might initiate a segregation of bacterial populations by substrate preferences, comparable to hydrolyzing model isolates (Zhu et al, 2016; Koch et al, 2019a) In this context, the CAZyme repertoire is considered to be a stronger driver of niche specialization than phylogenetic relationships (Hehemann et al, 2016; Wolter et al, 2021a). The identification of alginate as preferred substrate, whereas pectin primarily served as colonization scaffold, illuminates bacterial microhabitat ecology and substrate cycling in macroalgae-rich habitats with diverse polysaccharide budgets
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