Phosphate insensitive aminophosphonate mineralisation within oceanic nutrient cycles

Abstract

Many areas of the ocean are nutrient-poor yet support large microbial populations, leading to intense competition for and recycling of nutrients. Organic phosphonates are frequently found in marine waters, but require specialist enzymes for catabolism. Previous studies have shown that the genes that encode these enzymes in marine systems are under Pho regulon control and so are repressed by inorganic phosphate. This has led to the conclusion that phosphonates are recalcitrant in much of the ocean, where phosphorus is not limiting despite the degradative genes being common throughout the marine environment. Here we challenge this paradigm and show, for the first time, that bacteria isolated from marine samples have the ability to mineralise 2-aminoethylphosphonate, the most common biogenic marine aminophosphonate, via substrate-inducible gene regulation rather than via Pho-regulated metabolism. Substrate-inducible, Pho-independent 2-aminoethylphosphonate catabolism therefore represents a previously unrecognised component of the oceanic carbon, nitrogen and phosphorus cycles.

Phosphate‐limited ocean regions select for bacterial populations enriched in the carbon–phosphorus lyase pathway for phosphonate degradation

“…In contrast to the decline of C–P lyase in the MPZ, the phosphonate hydrolases encoded by phnA and phnX became relatively more abundant. This is consistent with previous surveys of phosphonate degradation functions and in support of the hypothesis that phosphonate degradation at these depths functions independently of Pi and is instead important to obtain C and N (Quinn et al ., ; Martínez et al ., ; Luo et al ., ; Chin et al ., ). Thus, the distribution of C–P lyase in the EPZ is strongly linked to Pi scarcity.…”

Elemental Composition, Phosphorous Uptake, and Characteristics of Growth of a SAR11 Strain in Batch and Continuous Culture

“…However, one potential class of DOP compounds receiving recent attention are phosphonates, which are organic phosphonic acid derivatives containing a C-P bond and which make up 25% of the high-molecular-weight DOM pool (21). Evidence of the widespread distribution of genes for the transport and metabolism of phosphonates has been reported in marine microorganisms (22–24) including SAR11 (see Table S1 in the supplemental material) (17, 19), and there is precedent for the PO 4 3− -independent utilization of phosphonates in marine systems (25). In laboratory experiments with a defined growth medium, SAR11 subgroup Ia strain HTCC7211 was shown to utilize phosphonates as a source of P for growth (12).…”

Transporter characterisation reveals aminoethylphosphonate mineralisation as a key step in the marine phosphorus redox cycle

“…in a Pi-insensitive manner, has been neglected. However, emerging evidence suggests that Pi-insensitive 2AEP catabolism occurs in nature 22 , 23 . Notably, the fact that 2AEP is either absent from, or a minor component of, otherwise phosphonate rich high molecular weight dissolved organic matter (HMW DOM) 16 , 17 , despite its supposed ubiquitous production 9 , 19 , 24 , 25 , suggests preferential catabolism of this molecule in comparison to alkylphosphonates.…”

“…In marine surface waters, genes encoding the C-P lyase are enriched in bacterial genomes found in regions typified by low Pi concentrations 20 where they are also heavily expressed 38 . Recent data has shown Pi-insensitive regulation of 2AEP degradation, facilitated by the 2AEP-specific systems, occurs in a few strains of bacteria related to marine Alphaproteobacteria 22 and a terrestrial gammaproteobacterium 23 . In both cases, a major consequence of Pi-insensitive 2AEP degradation was the remineralisation and release of labile Pi 22 , due to the greater cellular demand for N over P and the 1:1 N:P stoichiometry of 2AEP.…”