Ecosystem consequences of a nitrogen-fixing proto-organelle.

Abstract

Microscale symbioses can be critical to ecosystem functions, but the mechanisms of these interactions in nature are often cryptic. Here, we use a combination of stable isotope imaging and tracing to reveal carbon (C) and nitrogen (N) exchanges among three symbiotic primary producers that fuel a salmon-bearing river food web. Bulk isotope analysis, nanoSIMS (secondary ion mass spectrometry) isotope imaging, and density centrifugation for quantitative stable isotope probing enabled quantification of organism-specific C- and N-fixation rates from the subcellular scale to the ecosystem. After winters with riverbed-scouring floods, the macroalga <i>Cladophora glomerata</i> uses nutrients in spring runoff to grow streamers up to 10 m long. During summer flow recession, riverine N concentrations wane and <i>Cladophora</i> becomes densely epiphytized by three species of <i>Epithemia</i>, diatoms with N-fixing endosymbionts (proto-organelles) descended from a free-living <i>Crocosphaera</i> cyanobacterium. Over summertime epiphyte succession on <i>Cladophora</i>, N-fixation rates increased as <i>Epithemia</i> spp. became dominant, <i>Cladophora</i> C-fixation declined to near zero, and <i>Epithemia</i> C-fixation increased. Carbon transfer to caddisflies grazing on <i>Cladophora</i> with high densities of <i>Epithemia</i> was 10-fold higher than C transfer to caddisflies grazing <i>Cladophora</i> with low <i>Epithemia</i> loads. In response to demand for N, <i>Epithemia</i> allocates high levels of newly fixed C to its endosymbiont. Consequently, these endosymbionts have the highest rates of C and N accumulation of any taxon in this tripartite symbiosis during the biologically productive season and can produce one of the highest areal rates of N-fixation reported in any river ecosystem.