Microbial gardening in the ocean's twilight zone: detritivorous metazoans benefit from fragmenting, rather than ingesting, sinking detritus: fragmentation of refractory detritus by zooplankton beneath the euphotic zone stimulates the harvestable production of labile and nutritious microbial biomass

Abstract

Sinking organic particles transfer ∼10 gigatonnes of carbon into the deep ocean each year, keeping the atmospheric CO2 concentration significantly lower than would otherwise be the case. The exact size of this effect is strongly influenced by biological activity in the ocean's twilight zone (∼50-1,000 m beneath the surface). Recent work suggests that the resident zooplankton fragment, rather than ingest, the majority of encountered organic particles, thereby stimulating bacterial proliferation and the deep-ocean microbial food web. Here we speculate that this apparently counterintuitive behaviour is an example of 'microbial gardening', a strategy that exploits the enzymatic and biosynthetic capabilities of microorganisms to facilitate the 'gardener's' access to a suite of otherwise unavailable compounds that are essential for metazoan life. We demonstrate the potential gains that zooplankton stand to make from microbial gardening using a simple steady state model, and we suggest avenues for future research.

Keywords: carbon cycling; detritus; mesopelagic; microbial loop; nutrition; polyunsaturated fatty acid; zooplankton.

Figure 1

Microbial gardening in the twilight zone. We speculate that detritivorous zooplankton stimulate the production of labile and nutritious microbial biomass by fragmenting, rather than ingesting, large detrital particles. Detritus fragmentation increases the amount of organic matter exposed to bacterial degradation, encouraging their population growth. Increased bacterial biomass fuels the growth of flagellates and ciliates and the concomitant production of essential biochemical compounds. These protists, which are energetically and nutritionally superior to detritus, are sufficiently large to be effectively harvested by the zooplankton. Image not to scale.

Figure 2

Model-predictions illustrating how the proportion of large, fast sinking particles (D1) fragmented into smaller, slow- or non-sinking particles (D2) by detritivorous zooplankton (λ) affects their: A: Ingestion, B: Production, C: Gross growth efficiency, and D: Production when the absorption efficiency of D1 particles (β₁) is varied. The complete budget is presented in Supporting Information Fig. S3. Ingestion and production (panels A, B, and D) are scaled to relative to a detrital flux of 100 (nominal units) entering the twilight zone.