Due to their ability to degrade algal polysaccharides, they have thus been a primary focus of research ( Xing et al., 2015 Francis et al., 2019, 2021 Kappelmann et al., 2019 Krüger et al., 2019 Avcı et al., 2020). During the 2010–2012 spring algal blooms, members of the family Flavobacteriaceae were observed to be the most abundant and recurrent bacterial clade ( Teeling et al., 2016). Spring phytoplankton blooms in these shallow temperate waters are often dominated by diatoms ( Eisma, 1987 Giebel et al., 2011), with multiple studies reporting on the composition of bacterioplankton communities ( Eilers et al., 2000, 2001 Zubkov et al., 2001 Gerdts et al., 2004 Alderkamp et al., 2006 Rink et al., 2007). Helgoland Roads, a long-term ecological research station located in the German Bight of the North Sea hosts annual spring and summer blooms. Both DOM and POM consumption by bacteria contribute significantly to the biogeochemical cycles of carbon, nitrogen, and silicon ( Azam and Long, 2001), and lead to remineralization of organic matter back to inorganic constituents required for phytoplankton growth ( Bidle et al., 2002). These bacteria consume dissolved and particulate organic matter (DOM/POM) derived from both living and senescent/dead phytoplankton cells ( Smith et al., 1992). This ecosystem imbalance is accompanied by an increase in abundance and activity of heterotrophic bacteria ( Buchan et al., 2014). These blooms are transient, seasonal and localized events characterized by an increased abundance of algal cells and a spike in the assimilation of CO 2 and inorganic nutrients (nitrogen and phosphorus) ( Behrenfeld et al., 2005 Behrenfeld et al., 2006). Marine phytoplankton blooms are an essential part of ocean and global nutrient cycles. Altogether, these findings suggest that while many members of Rhodobacterales are competitive during diatom blooms, only a subset form close associations with diatoms by colonizing their phycospheres. In addition, putative phycosphere colonizers possessed higher prevalence of secondary metabolite biosynthetic gene clusters, particularly homoserine lactones, which can regulate bacterial attachment through quorum sensing. The defining feature of putative phycosphere colonizers is the presence of the tight adherence ( tad) gene cluster, which is responsible for the assembly of adhesive pili that presumably enable attachment to diatom hosts. In contrast, putative phycosphere colonizers exhibited large fluctuation in relative abundance across the different blooms and correlated strongly with particular diatom species that were dominant during the blooms each year. A closer examination of putative generalists and colonizers showed that putative generalists had persistently higher relative abundance throughout the blooms and thus produced more than 80% of Rhodobacterales transport proteins, suggesting rapid growth. Metaproteomes indicated that the species represented by these MAGs were the dominant suppliers of vitamin B 12 during the blooms, concomitant with a significant enrichment of genes related to vitamin B 12 biosynthesis suggestive of association with diatom phycospheres. They exhibited the highest gene enrichment and protein expression of small-molecule transporters, such as monosaccharides, thiamine and polyamine transporters, and anaplerotic pathways, such as ethylmalonyl and propanoyl-CoA metabolic pathways, all suggestive of a generalist lifestyle. Rhodobacterales metagenome assembled genomes (MAGs) were recurrently abundant. We investigated Rhodobacterales in the North Sea during the 2010–2012 spring blooms using a time series of 38 deeply sequenced metagenomes and 10 metaproteomes collected throughout these events. However, the molecular mechanisms that differentiate Rhodobacterales generalists and phycosphere colonizers are poorly understood. Many observations suggest that members of this clade are specialized in colonizing the microenvironment of diatom cells, known as the phycosphere. These photoheterotrophic bacteria have traditionally been described as generalists that scavenge dissolved organic matter. A prominent example of those is the consistent association of diatoms with Alphaproteobacteria of the order Rhodobacterales. The multiple interactions of phytoplankton and bacterioplankton are central for our understanding of aquatic environments.
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