The Role of Phosphorus Limitation in Shaping Soil Bacterial Communities and Their Metabolic Capabilities.

Angela M Oliverio,Krista Mcguire,Noah Fierer,Kristin Saltonstall,Benjamin L Turner,Andrew Bissett,Mary Ann Moran

doi:10.1128/mbio.01718-20

Abstract

Phosphorus (P) is an essential nutrient that is often in limited supply, with P availability constraining biomass production in many terrestrial ecosystems. Despite decades of work on plant responses to P deficiency and the importance of soil microbes to terrestrial ecosystem processes, how soil microbes respond to, and cope with, P deficiencies remains poorly understood. We studied 583 soils from two independent sample sets that each span broad natural gradients in extractable soil P and collectively represent diverse biomes, including tropical forests, temperate grasslands, and arid shrublands. We paired marker gene and shotgun metagenomic analyses to determine how soil bacterial and archaeal communities respond to differences in soil P availability and to detect corresponding shifts in functional attributes. We identified microbial taxa that are consistently responsive to extractable soil P, with those taxa found in low P soils being more likely to have traits typical of oligotrophic life history strategies. Using environmental niche modeling of genes and gene pathways, we found an enriched abundance of key genes in low P soils linked to the carbon-phosphorus (C-P) lyase and phosphonotase degradation pathways, along with key components of the high-affinity phosphate-specific transporter (Pst) and phosphate regulon (Pho) systems. Taken together, these analyses suggest that catabolism of phosphonates is an important strategy used by bacteria to scavenge phosphate in P-limited soils. Surprisingly, these same pathways are important for bacterial growth in P-limited marine waters, highlighting the shared metabolic strategies used by both terrestrial and marine microbes to cope with P limitation.

Highlights

Phosphorus (P) is an essential nutrient that is often in limited supply, with P availability constraining biomass production in many terrestrial ecosystems
The Acidobacteria, Solibacteraceae subgroup 3, and Acidobacteriales were consistently enriched in low P soils, and Planococcaceae were relatively more abundant in high P soils across the two study systems
Our estimates of maximum potential growth rates yielded additional evidence that increasing P availability tends to select for more copiotrophic bacterial taxa

Summary

Introduction

Phosphorus (P) is an essential nutrient that is often in limited supply, with P availability constraining biomass production in many terrestrial ecosystems. Using environmental niche modeling of genes and gene pathways, we found an enriched abundance of key genes in low P soils linked to the carbon-phosphorus (C-P) lyase and phosphonotase degradation pathways, along with key components of the high-affinity phosphate-specific transporter (Pst) and phosphate regulon (Pho) systems Taken together, these analyses suggest that catabolism of phosphonates is an important strategy used by bacteria to scavenge phosphate in P-limited soils. Much of the previous work on microbial responses to differences in soil P have relied on fertilization experiments [15, 16] where P availability is elevated by adding exogenous inputs of mineral P (typically high levels of calcium phosphate) These P dynamics likely do not reflect the conditions experienced by most organisms in natural ecosystems [17]. We know that lower P availability is associated with efficient phosphate uptake/transport systems and P starvation response regulation, but we do not know if these observed patterns are generalizable across a range of different soils and geographic locations

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