Abstract
Despite several studies reporting diazotrophic macroalgal associations (DMAs), biological nitrogen fixation (BNF) is still largely overlooked as a potential source of nitrogen (N) for macroalgal productivity. We investigated the role of BNF, via the acetylene reduction method, throughout different life stages of the invasive macroalga, Sargassum horneri, in its non-native Southern California coastal ecosystem. Throughout most of its life cycle, BNF rates were not detectable or yielded insignificant amounts of fixed N to support S. horneri productivity. However, during late summer when nutrient concentrations are usually at their minimum, BNF associated with juvenile S. horneri contributed ∼3–36% of its required N, potentially providing it with a competitive advantage. As DMAs remain poorly understood within macroalgal detrital systems, long term (15–28 days) laboratory decomposition time series were carried out to investigate the role of BNF throughout decomposition of the endemic macroalga, S. palmeri, and the invasive S. horneri. Nitrogenase activity increased drastically during the second phase of decomposition, when increasing microbial populations are typically thought to drive macroalgal degradation, with BNF rates associated with S. palmeri and S. horneri reaching up to 65 and 247 nmol N × g-1(dw) × h-1, respectively. Stimulation of BNF rates by glucose and mannitol additions, up to 42× higher rates observed with S. palmeri, suggest that labile carbon may be limiting at varying degrees in these detrital systems. Comparable, if not higher, dark BNF rates relative to light incubations during S. horneri decomposition suggest an important contribution from heterotrophic N fixers. Inhibition of nitrogenase activity, up to 98%, by sodium molybdate additions also suggest that sulfate reducers may be an important constituent of the detrital diazotrophic community. As labile N can become limiting to the microbial community during macroalgal decomposition, our results suggest that BNF may provide a source of new N, alleviating this limitation. Additionally, while BNF is rarely considered as a source for N enrichment with aging macroalgal detritus, we found it to account for ∼1–11% of N immobilized with decaying S. horneri. Our investigations suggest that DMAs may be globally important with Sargassum and potentially occur within other macroalgal detrital systems.
Highlights
Benthic and pelagic marine macroalgae, encompassing three divisions (Rhodophyta, Chlorophyta, Phaeophyceae), are a diverse group of photoautotrophic organisms that extend across polar, temperate, and tropical latitudes (Keith et al, 2014)
Seasonal biological nitrogen fixation (BNF) rates associated with freshly collected S. horneri (Supplementary Table S2) yielded significantly lower rates than those associated with decomposing macroalgal detritus (Supplementary Tables S3, S4)
Higher BNF rates [∼12–24 nmol N × g−1 × h−1] associated with freshly collected S. horneri were measured in the summer when necrosis was already beginning to take place with the seaweed upon time of collection
Summary
Benthic and pelagic marine macroalgae, encompassing three divisions (Rhodophyta, Chlorophyta, Phaeophyceae), are a diverse group of photoautotrophic organisms that extend across polar, temperate, and tropical latitudes (Keith et al, 2014). Species of brown macroalgae from the genus Sargassum truly highlight this cosmopolitan distribution as they occur in diverse benthic habitats along coastal zones throughout the world, spanning from the Gulf of California (Pacheco-Ruíz et al, 1998) to the rocky intertidal shores of the Japan Sea (Umezaki, 1984), occur in coral reefs such as the Great Barrier Reef (McCook, 1997) and form pelagic communities throughout the Sargasso Sea, Gulf of Mexico, and Gulf Stream (Butler and Stoner, 1984). Benthic macroalgae can make important seasonal contributions to primary productivity in nearshore fringing reefs of the central Great Barrier Reef (Schaffelke and Klumpp, 1997) and dominate productivity along coastal ecosystems, contributing up to 50% of global coastal gross primary production (Duarte et al, 2005). Primary production by macroalgae provides fixed carbon to other organisms through leaching of dissolved organic carbon or direct grazing, the vast majority of macroalgal production (estimates up to 90%; Mann, 1973) enters the detrital food chain or is sequestered in marine sediments or the deep ocean (Krause-Jensen and Duarte, 2016)
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