Community Proteogenomics Reveals the Systemic Impact of Phosphorus Availability on Microbial Functions in Tropical Soil

Microbial communities optimize their effort acquiring rare nutrients in nutrient-deficient tropical soils.

Like Comment

The paper in Nature Ecology & Evolution is here:

Phosphorus is a key limiting nutrient, particularly in humid tropical forests, where many years of high rainfall leads to strongly weathered soils that are leached of phosphorus and other nutrients.  Phosphorus strongly associates with aluminum- and iron-containing soil minerals that are abundant in tropical forest soils, limiting its availability for plants and microbes. Lack of available phosphorus therefore limits productivity in many tropical regions.

Ecological theories suggest that an efficient community will adjust its foraging strategy to balance the distribution of life-sustaining elements carbon, nitrogen, phosphorus, and sulfur, and thereby emphasize the acquisition of rare nutrients and minimize the acquisition of available nutrients. Communities allocate resources for phosphorus acquisition using this approach – by producing simple enzymes like phosphomonoesterases to acquire easily accessible forms of phosphorus, versus more complex enzymes like phytase to acquire the most complex forms of phosphorus.

The Smithsonian Tropical Research Institute’s long-term fertilization experiment in Panama provided a perfect place to test these theories on soil microbial communities. Phosphorus and other nutrients have been added to the experimental plots every year since 1998. We collected soils from untreated control and phosphorus addition plots, and performed a suite of analyses to probe microbial genetic differences between the two treatments. We teamed with the Joint Genome Institute to conduct very deep sequencing of soil metagenomes, and used mass spectrometry at Oak Ridge National Laboratory (ORNL) to identify > 7,000 proteins in each soil sample. Supercomputers in Oak Ridge Leadership Computing Facility enabled analysis of the massive –omics datasets. Pacific Northwest National Laboratory’s Environmental Molecular Sciences Laboratory added molecular characterization of soil organic matter using ultra-high-resolution mass spectrometry.

We found distinct differences in microbial genes and proteins between the phosphorus-rich and phosphorus-poor soils. Genes to produce phosphorus-acquiring enzymes were much more numerous in the phosphorus-deficient untreated soils. Further, we found > 100 genes associated with acquiring phosphorus from phytate, which is a complex organic compound derived from plant litter. Finding so many genes to break apart and transport such a complex molecule tells us that microbes are extremely hungry for phosphorus in the untreated soil. Some organisms acquire phosphorus from phytate while others acquire it from other organic phosphorus compounds, proving that soil microbes can partition nutrient acquisition within the community.  

We also identified differences between the phosphorus-deficient and phosphorus-rich soils for genes involved in the carbon, nitrogen, and sulfur cycles. In particular, the phosphorus-rich soil contained much lower abundance of genes for phosphorus acquisition, but many more genes for the breakdown of complex carbon compounds. This demonstrates that when phosphorus was plentiful, the microbial community prioritized the breakdown of other needed compounds, focusing its effort on the most limiting element to balance its nutritional needs. These findings help understand how soil microbial communities adjust to nutrient-poor soils, and have applications in agriculture and terrestrial biosphere modeling.

Melanie Mayes

Senior Staff Scientist, Oak Ridge National Laboratory