TY - JOUR
T1 - The role of phosphorus limitation in shaping soil bacterial communities and their metabolic capabilities
AU - Oliverio, Angela M.
AU - Bissett, Andrew
AU - McGuire, Krista
AU - Saltonstall, Kristin
AU - Turner, Benjamin L.
AU - Fierer, Noah
N1 - Funding Information:
We also acknowledge the contribution of the Australian Microbiome consortium in the generation of data used in this publication. The Australian Microbiome initiative is supported by funding from Bioplatforms Australia and the Integrated Marine Observing System (IMOS) through the Australian Government’s National Collaborative Research Infrastructure Strategy (NCRIS), Parks Australia through the Bush Blitz program funded by the Australian Government and BHP, and the CSIRO.
Funding Information:
This research was partially supported by a grant from the Simons Foundation to the Smithsonian Tropical Research Institute (429440) and a grant to N.F. from the U.S. National Science Foundation (DEB 1556090). A.M.O. acknowledges support from an NSF Graduate Research Fellowship and NSF Graduate Research Internship Program Fellowship.
Publisher Copyright:
© 2020 Oliverio et al.
PY - 2020/9/1
Y1 - 2020/9/1
N2 - 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 grass-lands, 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 oligo-trophic 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.
AB - 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 grass-lands, 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 oligo-trophic 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.
KW - C-P lyase pathway
KW - Organophosphonate degradation
KW - Phosphate starvation
KW - Phosphorus limitation
KW - Soil microbiology
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U2 - 10.1128/mBio.01718-20
DO - 10.1128/mBio.01718-20
M3 - Article
C2 - 33109755
AN - SCOPUS:85094808308
SN - 2161-2129
VL - 11
SP - 1
EP - 16
JO - mBio
JF - mBio
IS - 5
M1 - e01718-20
ER -