Microbial Phosphorus Mobilization Strategies Across a Natural Nutrient Limitation Gradient and Evidence for Linkage with Iron Solubilization Traits
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Lawrence Berkeley National Laboratory Recent Work Title Microbial Phosphorus Mobilization Strategies Across a Natural Nutrient Limitation Gradient and Evidence for Linkage With Iron Solubilization Traits. Permalink https://escholarship.org/uc/item/9gr0v2jb Authors Wang, Shi Walker, Robert Schicklberger, Marcus et al. Publication Date 2021 DOI 10.3389/fmicb.2021.572212 Peer reviewed eScholarship.org Powered by the California Digital Library University of California fmicb-12-572212 June 18, 2021 Time: 11:2 # 1 ORIGINAL RESEARCH published: 23 June 2021 doi: 10.3389/fmicb.2021.572212 Microbial Phosphorus Mobilization Strategies Across a Natural Nutrient Limitation Gradient and Evidence for Linkage With Iron Solubilization Traits Shi Wang1*, Robert Walker1,2, Marcus Schicklberger1†, Peter S. Nico3, Patricia M. Fox3, Ulas Karaoz1, Romy Chakraborty1 and Eoin L. Brodie1,4* 1 Ecology Department, Climate and Ecosystem Sciences Division, Earth and Environmental Sciences Area, Lawrence Edited by: Berkeley National Laboratory, Berkeley, CA, United States, 2 School of BioSciences, University of Melbourne, Parkville, VIC, Steffen Kolb, Australia, 3 Energy Geosciences Division, Earth and Environmental Sciences Area, Lawrence Berkeley National Laboratory, Leibniz Centre for Agricultural Berkeley, CA, United States, 4 Department of Environmental Science, Policy and Management, University of California, Landscape Research (ZALF), Berkeley, Berkeley, CA, United States Germany Reviewed by: Microorganisms have evolved several mechanisms to mobilize and mineralize occluded Stefanie Schulz, Helmholtz Zentrum München, and insoluble phosphorus (P), thereby promoting plant growth in terrestrial ecosystems. Helmholtz-Gemeinschaft Deutscher However, the linkages between microbial P-solubilization traits and the preponderance Forschungszentren (HZ), Germany of insoluble P in natural ecosystems are not well known. We tested the P solubilization Eva Lehndorff, University of Bayreuth, Germany traits of hundreds of culturable bacteria representative of the rhizosphere from a natural *Correspondence: gradient where P concentration and bioavailability decline as soil becomes progressively Shi Wang more weathered. Aluminum, iron phosphate and organic P (phytate) were expected to [email protected] Eoin L. Brodie dominate in more weathered soils. A defined cultivation medium with these chemical [email protected] forms of P was used for isolation. A combination of soil chemical, spectroscopic †Present address: analyses and 16S rRNA gene sequencing were used to understand the in situ ability Marcus Schicklberger, for solubilization of these predominant forms of P. Locations with more occluded and Pendulum Therapeutics, San Francisco, CA, United States organic P harbored the greatest abundance of P-mobilizing microorganisms, especially Burkholderiaceae (Caballeronia and Paraburkholderia spp.). Nearly all bacteria utilized Specialty section: This article was submitted to aluminum phosphate, however fewer could subsist on iron phosphate (FePO4) or Terrestrial Microbiology, phytate. Microorganisms isolated from phytic acid were also most effective at solubilizing a section of the journal FePO4, suggesting that phytate solubilization may be linked to the ability to solubilize Frontiers in Microbiology Fe. Significantly, we observed Fe to be co-located with P in organic patches in soil. Received: 13 June 2020 Accepted: 12 March 2021 Siderophore addition in lab experiments reinstated phytase mediated P-solubilization Published: 23 June 2021 from Fe-phytate complexes. Taken together, these results indicate that metal-organic-P Citation: complex formation may limit enzymatic P solubilization from phytate in soil. Additionally, Wang S, Walker R, Schicklberger M, Nico PS, Fox PM, the linked traits of phytase and siderophore production were mostly restricted to specific Karaoz U, Chakraborty R and clades within the Burkholderiaceae. We propose that Fe complexation of organic P (e.g., Brodie EL (2021) Microbial phytate) represents a major constraint on P turnover and availability in acidic soils, as Phosphorus Mobilization Strategies Across a Natural Nutrient Limitation only a limited subset of bacteria appear to possess the traits required to access this Gradient and Evidence for Linkage persistent pool of soil P. With Iron Solubilization Traits. Front. Microbiol. 12:572212. Keywords: phosphorus limitation, phosphorus mobilization, microbial traits, iron complexed organic phosphorus, doi: 10.3389/fmicb.2021.572212 siderophores Frontiers in Microbiology| www.frontiersin.org 1 June 2021| Volume 12| Article 572212 fmicb-12-572212 June 18, 2021 Time: 11:2 # 2 Wang et al. Microbial Phosphorus Mobilization Traits INTRODUCTION and Al bridges, or co-precipitated as a metal-organic P complex it is less susceptible to direct enzymatic hydrolysis (Veinot and Phosphorus (P) is one of the most limiting plant nutrients, with Thomas, 1972; Dao, 2003; He et al., 2006). Therefore to access P in yield on 30–40% of the world’s arable land limited by P availability Al/Fe complexed phytic acid, microbes likely need to coordinate (Runge-Metzger, 1995; Nesme et al., 2018). During soil formation multiple metabolic strategies such as ligand and enzyme secretion and aging (pedogenesis), P weathers from a mineral form to a to mobilize insoluble P. 3− labile form (dissolved orthophosphate, PO4 ) that is available To date, research has focused more on the biological for plant uptake. However, much of the labile P becomes sorbed availability of inorganic rather than organic P (Jones and onto mineral surfaces, immobilized into soil organic matter, or Oburger, 2011; Gerke, 2015; Alori et al., 2017). However, both incorporated into recalcitrant inorganic forms. These processes soil pH and soil mineralogy are key regulators of P solubility and result in eventual depletion of labile P with an accumulation the study of microbial P solubilization must consider the primary of the occluded and organic forms of P that are not readily in vitro forms of P to which the indigenous microbiome may accessible to plants (Izquierdo et al., 2013; George et al., 2018). have adapted. Our study focused initially on the mobilization of P The organic P fraction of which phytate (inositol phosphate) is from both organic (phytate) and inorganic (aluminum and iron frequently a major component (McKercher and Anderson, 1989; phosphate) forms that were expected to dominate at our study Turner et al., 2006), can account for 20–95% of total P (Dalai, site, termed “The Ecological Staircase.” 1977; Stewart and Tiessen, 1987). The fixation and subsequent The “Ecological Staircase” (ES) in Mendocino County, immobilization of phytate in soil is often much stronger than California also known as the Hans Jenny Pygmy Forest Reserve, that of the orthophosphate anions (McKercher and Anderson, is part of the University of California, Natural Reserve System. 1989), however, the reasons for the accumulation of phytate in It represents a soil chronosequence exhibiting extreme nutrient soil are not fully clear. Owing to its high negative charge, phytate limitation across a gradient comprised of five wave-cut marine is tightly adsorbed to various soil components (Lung and Lim, terraces (T1–T5) formed through wave-action and elevated 2006) and the sorption of phytate to soil solid phases has been through tectonic activity (Jenny et al., 1969; Westman and shown to induce the formation of Fe/Al-phytate precipitates Whittaker, 1975; Yu et al., 2003; Izquierdo et al., 2013). Soils at oxide surfaces (Celi and Barberis, 2005; Yan et al., 2014), on the older terraces (T3–T5) have been intensively weathered, or the formation of humic-Fe(Al)-phytate complexes at humic becoming enriched in Fe and Al oxides resulting in highly surfaces via Fe or Al bridges (He et al., 2006; Gerke, 2010; leached spodosols and ultisols with lower fertility and higher Chen et al., 2018). acidity than the younger terraces dominated by inceptisols and To access P of various forms, plants are aided by the growth ultisols (Northup et al., 1998; Yu et al., 2003). Consequently, and activity of soil microorganisms, which possess metabolic soil development and therefore the distribution of P between mechanisms to mineralize and mobilize plant inaccessible the organic and inorganic pools, as well as the composition of P P into orthophosphate by (1) enhanced dissolution of P forms, have a major impact on P accessibility for both plants and containing minerals through soil acidification or release of microorganisms. Such a gradient over a relatively short distance metal chelating ligands e.g., organic acids, siderophores, etc. (∼3 miles) represents an ideal system to study the adaptation of (Khan et al., 2014; Alori et al., 2017); (2) secretion of soil microbes in response to severe nutrient stress. extracellular enzymes to mineralize organic P (Rodríguez and Previous work investigating P availability at the Ecological Fraga, 1999; Sharma et al., 2013; Alori et al., 2017), and Staircase (Northup et al., 1995; Izquierdo et al., 2013; Uroz (3) reductive dissolution of Fe(Al)-complexed organic P (He et al., 2014) set the basis for our study. With an accumulation et al., 2006; Chen et al., 2018). Although, a number of of the occluded and organic forms of P, P becomes a primary organisms e.g., Pseudomonas, Burkholderia, and Bacillus spp. limiting nutrient in older terraces. Uroz et al.(2014) addressed have been identified as phosphate-solubilizing bacteria (PSB), the relationship between nutrient availability