Rapid nitrogen fixation by canopy microbiome in tropical forest determined by both phosphorus and molybdenum

Abstract

Biological nitrogen fixation is critical for the nitrogen cycle of tropical forests, yet we know little about the factors that control the microbial nitrogen fixers that colonize the microbiome of leaves and branches that make up a forest canopy. Forest canopies are especially prone to nutrient limitation because they are (1) disconnected from soil nutrient pools and (2) often subject to leaching. Earlier studies have suggested a role of phosphorus and molybdenum in controlling biological N‐fixation rates, but experimental confirmation has hitherto been unavailable. Here we present the results of a manipulation of canopy nutrient availability. Our findings demonstrate a primary role of phosphorus in constraining overall N fixation by canopy cyanobacteria, but also a secondary role of molybdenum in determining per‐cell fixation rates. A conservative evaluation suggests that canopy fixation can contribute to significant N fluxes at the ecosystem level, especially as bursts following atmospheric inputs of nutrient‐rich dust.

Molybdenum, phosphorus, and pH do not constrain nitrogen fixation in a tropical forest in the southeastern Amazon

“…When we did see responses, they occurred 1 d after Mo and P applications to soil during the dry season and 1 month after applications of Mo, P, and lime combined in the wet season. Our results were unexpected, given that all previous studies that tested Mo or P limitation on BNF in the tropics have demonstrated more prominent responses to Mo (Barron et al 2009, Winbourne et al 2017, to P Hobbie 2000, Reed et al 2013), or to both (Wurzburger et al 2012, Stanton et al 2019. This was particularly surprising considering that Mo limitation is seemingly widespread in temperate and boreal ecosystems (Horstmann et al 1982, Silvester 1989, Jean et al 2013, Rousk et al 2016, Perakis et al 2017, P erez et al 2017, spanning from temperate regions of relatively high Mo richness and deposition (Marks et al 2015, Perakis et al 2017 to boreal systems with relatively low Mo FIG.…”

“…The southeastern Amazon is a region where Mo and P limitation may be pronounced because soils are developed from old, stable surfaces with little to no parent material contribution (Quesada et al 2011) and where atmospheric inputs are very low (Mahowald et al 2008, Wong et al 2020 a ). While a handful of studies have assessed the simultaneous effects of Mo and P on free‐living BNF rates in the tropics, such as in Hawaii, Panama, Costa Rica, and Belize (Vitousek and Hobbie 2000, Barron et al 2009, Wurzburger et al 2012, Reed et al 2013, Winbourne et al 2017, Stanton et al 2019), these regions have higher weathering and atmospheric inputs, particularly from sea‐salt aerosols (Wong et al 2020 a ). In addition, these studies have either been short‐term experiments testing the addition of Mo and or P, or longer‐term studies with Mo added as a nutrient “cocktail” where responses to Mo alone have not been examined (Vitousek and Hobbie 2000, Barron et al 2009).…”

Specialized bacteriome uncovered in the coralloid roots of the epiphytic gymnosperm, Zamia pseudoparasitica

“…Epiphytes face several constraints regarding nutrient acquisition, and the microbial community seems to provide a good dose of crucial elements such as fixed nitrogen (Stanton et al, 2019).…”

“…Epiphytes face several constraints regarding nutrient acquisition, and the microbial community seems to provide a good dose of crucial elements such as fixed nitrogen (Stanton et al, ). The presence of endophytic bacteria within the coralloid roots of Z. pseudoparasitica , many of whom have the potential to fix nitrogen, suggests that the species has an additional supply of nutrients in the challenging conditions that these epiphytes exist in.…”

“…However, plant genotype, developmental stage, and habitat also influence the composition of the microbial community found in the rhizobiome (Lundberg et al, 2012). Most plants have relatively easy access to soil nutrients and microbes; however, canopy epiphytes are exposed to a much harsher environment and face several unique constraints regarding nutrient acquisition: They are disconnected from soil nutrients and thus have to rely on nutrients leached by precipitation (rain or mist), nutrient-rich dusts, association with invertebrates (e.g., ants), vertebrates (e.g., treefrogs), and microbes found either epiphytically or endophytically (Chomicki & Renner, 2019;Okin, Mahowald, Chadwick, & Artaxo, 2004;Romero et al, 2010;Stanton, Bateman, Von Fischer, & Hedin, 2019). Three elements that typically limit growth in tropical epiphytes are phosphorus, nitrogen, and molybdenum (Barron et al, 2009;Stanton et al, 2019).…”