Emergent biogeochemical function in seagrass–sponge holobionts: evidence from a Mediterranean case study

Ulisse Cardini
1*
1
Department of Integrative Marine Ecology - Genoa Marine Center, Stazione Zoologica Anton Dohrn, Villa del Principe, Piazza del Principe 4, Genova, GE - 16031, Italia

Marine foundation species such as seagrasses structure coastal ecosystems not only through their physical architecture but through the metabolic activities of their associated microbiomes. The holobiont framework — which considers the host and its microbial partners as a single ecological and evolutionary unit — predicts that intimate species associations may give rise to emergent properties: collective functions that exceed the sum of individual contributions. Testing this prediction in natural systems, however, requires simultaneous characterisation of multiple biogeochemical processes across the partners in isolation and in combination.

In the Mediterranean Sea, the demosponge Chondrilla nucula is frequently found in Posidonia oceanica meadows, and the two organisms together with their respective microbiomes often co-occur in close physical contact. Whether this spatial association translates into a functionally integrated unit with distinct biogeochemical properties remains an open question. Here, we address this by characterising the full nitrogen-cycling repertoire of P. oceanica, C. nucula, and their association using ¹⁵N tracer incubations (¹⁵N₂, ¹⁵NH₄⁺, ¹⁵NO₃⁻), nutrient flux measurements, and 16S rRNA and metagenomic profiling across two seasons. We show that the association expresses a suite of microbial N-cycling functions — including N₂ fixation, nitrification, and nitrification-coupled denitrification — that cannot be predicted from the partners in isolation, and that sponge-mediated nitrification can support a significant fraction of seagrass nitrogen demand. Metagenomic data provide independent genomic support for the breadth of the association's N-cycling repertoire. Collectively, our results are consistent with the emergence of an integrated biogeochemical unit that enhances internal nitrogen retention and may buffer seagrass productivity against the oligotrophic conditions typical of the Mediterranean.

Reti trofiche, funzionamento degli ecosistemi ed ecologia di comunità
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