Abstract Seed banks are believed to contribute to compositional changes within and across microbial assemblages, but the application of this concept to natural communities remains challenging. Here we describe the core seed bank of a bacterial metacommunity from a boreal watershed, using the spatial distribution of bacterial operational taxonomic units (OTUs) across 223 heterogeneous terrestrial, aquatic and phyllosphere bacterial assemblages. Taxa were considered potential seeds if they transitioned from rare to abundant somewhere within the metacommunity and if they were ubiquitous and able to persist under unfavorable conditions, the latter assessed by checking their presence in three deeply sequenced samples (one soil, one river and one lake, 2.2–3 million reads per sample). We show that only a small fraction (13%) of all detected OTUs constitute a metacommunity seed bank that is shared between all terrestrial and aquatic communities, but not by phyllosphere assemblages, which seem to recruit from a different taxa pool. Our results suggest directional recruitment driven by the flow of water in the landscape, since most aquatic sequences were associated to OTUs found in a single deeply-sequenced soil sample, but only 45% of terrestrial sequences belonged to OTUs found in the two deeply-sequenced aquatic communities. Finally, we hypothesize that extreme rarity, and its interplay with water residence time and growth rates, may further constrain the size of the potential seed bank.