How To Live with Phosphorus Scarcity in Soil and Sediment: Lessons from Bacteria

Abstract

Phosphorus (P) plays a fundamental role in the physiology and biochemistry of all living things. Recent evidence indicates that organisms in the oceans can break down and use P forms in different oxidation states (e.g., ؉5, ؉3, ؉1, and ؊3); however, information is lacking for organisms from soil and sediment. The Cuatro Ciénegas Basin (CCB), Mexico, is an oligotrophic ecosystem with acute P limitation, providing a great opportunity to assess the various strategies that bacteria from soil and sediment use to obtain P. We measured the activities in sediment and soil of different exoenzymes involved in P recycling and evaluated 1,163 bacterial isolates (mainly Bacillus spp.) for their ability to use six different P substrates. DNA turned out to be a preferred substrate, comparable to a more bioavailable P source, potassium phosphate. Phosphodiesterase activity, required for DNA degradation, was observed consistently in the sampled-soil and sediment communities. A capability to use phosphite (PO 3 3؊ ) and calcium phosphate was observed mainly in sediment isolates. Phosphonates were used at a lower frequency by both soil and sediment isolates, and phosphonatase activity was detected only in soil communities. Our results revealed that soil and sediment bacteria are able to break down and use P forms in different oxidation states and contribute to ecosystem P cycling. Different strategies for P utilization were distributed between and within the different taxonomic lineages analyzed, suggesting a dynamic movement of P utilization traits among bacteria in microbial communities. IMPORTANCEPhosphorus (P) is an essential element for life found in molecules, such as DNA, cell walls, and in molecules for energy transfer, such as ATP. The Valley of Cuatro Ciénegas, Coahuila (Mexico), is a unique desert characterized by an extreme limitation of P and a great diversity of microbial life. How do bacteria in this valley manage to obtain P? We measured the availability of P and the enzymatic activity associated with P release in soil and sediment. Our results revealed that soil and sediment bacteria can break down and use P forms in different oxidation states and contribute to ecosystem P cycling. Even genetically related bacterial isolates exhibited different preferences for molecules, such as DNA, calcium phosphate, phosphite, and phosphonates, as substrates to obtain P, evidencing a distribution of roles for P utilization and suggesting a dynamic movement of P utilization traits among bacteria in microbial communities. P hosphorus (P) is an essential element for the synthesis of many biomolecules, including DNA, RNA, and ATP (1), with no substitute as a building block of life. P is also frequently limiting for a variety of biota, including vascular plants, marine and freshwater phytoplankton, aquatic and terrestrial bacteria, and herbivorous animals (2); thus, understanding how P limitation shapes ecological and evolutionary dynamics is a key step in linking levels of biological organization from genes to ecosystems.Or...

Two Pseudomonas aeruginosa clonal groups belonging to the PA14 clade are indigenous to the Churince system in Cuatro Ciénegas Coahuila, México

“…Moreover, the extreme unbalanced nutrimental stoichiometry where the ratio of nitrogen/phosphorous is very high (Elser et al, 2005;Lee et al, 2015Lee et al, , 2017 can explain most of the endemicity due to extreme selective pressure. It has been proposed that within CCB, oligotrophy not only forces the collaboration within the community to optimize its nutrient cycling (Tapia-Torres et al, 2016;Gomez-Lunar et al, 2018;Rodríguez-Torres et al, 2017), but it acts as an effective sieve against migration .…”

Agricultural land-use change in a Mexican oligotrophic desert depletes ecosystem stability

“…This situation is critical for the soils of CCB, because they contain a high diversity of native species that can face up the scarcity of nutrients, mainly P (Tapia-Torres et al, 2016). The organic agriculture with low pesticide inputs and the use of native microbial strains with different capabilities to use, transform and recycle the soil nutrients (i.e., phosphorus solubilizing bacteria) could be the best solution for agriculture in this particular and highly diverse important ecosystem.…”

Critical Review of Polyphosphate and Polyphosphate Accumulating Organisms for Agricultural Water Quality Management

“…For example, fungal and bacterial amendments increase P availability to crops by mobilizing soil-bound P (Hayat et al, 2010;Javot et al, 2007;P. Jeffries et al, 2003;Richardson et al, 2011;Richardson & Simpson, 2011;Rodríguez & Fraga, 1999;Tapia-Torres et al, 2016). There are only a few agricultural water quality best management practices that facilitate P retention via biological mechanisms (Table S3).…”