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 (PO3 (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.

Importance: Phosphorus (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.

FIG 1

Differences in the frequency of utilization of P sources among soil and sediment isolates. The y axis reports the proportion of isolates able to grow under each of the six different phosphorus sources. PP, potassium phosphate; CP, calcium phosphate; Phi, phosphite; 2-PA, 2-phosphonoacetaldehyde; 2-AEP, (2-aminoethyl)phosphonic acid. Isolates tested were recovered from Churince soil (CH), Pozas Azules soil (PA), Churince sediment (S), or fertilized sediment (FS). Since some isolates can grow under more than one P source, the proportion does not add to 1. All three factors were highly significant (P < 0.0001).

FIG 2

Distribution of phosphorus utilization capabilities among isolates of different taxonomic groups from soil and sediment communities. Phylogeny based on the 16S rRNA gene. The site of isolation is shown in the innermost circle, labeled 1 with the following colors: blue, Pozas Azules soil; red, Churince soil; dark green, Churince sediment; and light green, Churince fertilized sediment. The outer circles indicate the isolates' ability to grow with a given P source (represented in dark gray); light gray indicates lack of growth of the isolate. The circle numbers refer to P source evaluated: 2, potassium phosphate; 3, calcium phosphate; 4, phosphite; 5, 2-phosphonoacetaldehyde; 6, (2-aminoethyl)phosphonic acid; 7, DNA; and 8, P free.

FIG 3

Phosphorus source preferences by bacteria related to B. cereus sensu lato species. This is a closeup of the clade that groups Bacillus cereus, Bacillus thuringiensis, and Bacillus anthracis in Fig. 2. Phylogeny is based on the 16S rRNA gene. The site of isolation is shown in the innermost circle, labeled 1 and indicated by the following colors: blue, Pozas Azules soil; red, Churince soil; dark green, Churince sediment; and light green, Churince fertilized sediment. The outer circles indicate the isolates' ability to grow with a given P source (represented in dark gray); light gray indicates lack of growth of the isolate. The circle numbers refer to P source evaluated: 2, potassium phosphate; 3, calcium phosphate; 4, phosphite; 5, 2-phosphonoacetaldehyde; 6, (2-aminoethyl)phosphonic acid; 7, DNA; 8, P free.

FIG 4

Assortment of genotypes according to ecological similarity. The analysis was done with AdaptML (51). The 16S rRNA gene sequences are associated with colored bars in the outer ring that represent the sites of isolation (sediment or soil). The predictive model projected two habitats (1 and 2), shown in the inner circles on the phylogenetic branches as dots colored in yellow or purple, which reflect trends in distribution. Taxonomic assignments are shown on the outside based on type strain's sequences included in the analysis. Shown with bars at the left is the distribution of each population among isolation sites for each predicted habitat. Notice that habitat 2 groups most of the sediment isolates (dark green).