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

Abstract

The planktonic synthesis of reduced organophosphorus molecules, such as alkylphosphonates and aminophosphonates, represents one half of a vast global oceanic phosphorus redox cycle. Whilst alkylphosphonates tend to accumulate in recalcitrant dissolved organic matter, aminophosphonates do not. Here, we identify three bacterial 2-aminoethylphosphonate (2AEP) transporters, named AepXVW, AepP and AepSTU, whose synthesis is independent of phosphate concentrations (phosphate-insensitive). AepXVW is found in diverse marine heterotrophs and is ubiquitously distributed in mesopelagic and epipelagic waters. Unlike the archetypal phosphonate binding protein, PhnD, AepX has high affinity and high specificity for 2AEP (Stappia stellulata AepX Kd 23 ± 4 nM; methylphosphonate Kd 3.4 ± 0.3 mM). In the global ocean, aepX is heavily transcribed (~100-fold>phnD) independently of phosphate and nitrogen concentrations. Collectively, our data identifies a mechanism responsible for a major oxidation process in the marine phosphorus redox cycle and suggests 2AEP may be an important source of regenerated phosphate and ammonium, which are required for oceanic primary production.

A widely distributed phosphate-insensitive phosphatase presents a route for rapid organophosphorus remineralization in the biosphere

“…during Pi-replete or Pi-deplete growth conditions ( 24 ), we show that this enzyme is responsible for the rapid conversion of various natural organophosphorus substrates into bioavailable Pi independently of P availability. Thus, we reveal another widespread Pi-insensitive mechanism for the rapid conversion of organophosphorus into bioavailable P ( 42 , 43 ), which may explain why PME activity is detected in Pi-replete oceanic regions ( 4 , 44 , 45 ). Significantly, unlike genes encoding the canonical PMEs, phoX , phoD , and phoA , pafA distribution and transcription in seawater are almost exclusively affiliated with Bacteroidetes , which frequently associate with phytoplankton and sinking particles ( 46 , 47 ), suggesting that this phylum plays an overlooked and potentially major role in remineralizing labile Pi.…”

Comparative transcriptomics unveil distinctive metabolic pathway of phosphonate utilization by diatom Phaeodactylum tricornutum

“…Barely detectable DIP in 2-AEP culture suggested 2-AEP was transported into the cells to be utilized. However, genes coding phosphonate transporters PhnCDE, PhnSTU, AepXVW, AepP and AepSTU reported previously [16] were not identified in all examined groups (absence in the transcriptome). Instead, through integrated analysis, we deduced that 2-AEP was transported into cells encapsuled by the clathrin-coated vesicles.…”

“…In the light of many previous studies, bacteria and cyanobacteria are able to utilize 2-AEP by cleaving the C-P bond of 2-AEP to form phosphate [15, 16]. In contrast, the 2-AEP utilization mechanism of eukaryotic P. tricornutum unveiled in this study is disparate.…”

“…Phosphonates can be an alternative P source to microorganisms [14]. Although the utilization mostly occurs in phosphate-limited ocean regions, 2-AEP can be adopted by prokaryotes when DIP is sufficient as well [15, 16]. Catabolism of 2-AEP have been well elaborated in prokaryotes employing diverse pathways mediated by C-P lyase and C-P hydrolyses respectively [17, 18].…”

2‐Aminoethylphosphonate utilization in Pseudomonas putida BIRD‐1 is controlled by multiple master regulators

“…2‐aminoethylphosphonate (2AEP) is considered the most abundant phosphonate in nature (White and Metcalf, 2004) although to our knowledge in situ analytical estimates are lacking. Our previous work identified three transporters responsible for 2AEP uptake in the soil rhizobacteria Pseudomonas putida BIRD‐1 (hereafter BIRD‐1) (Murphy et al ., 2021). Two of these are ABC transporters, AepXVW and AepSTU, whilst the third, AepP, is a member of the organophosphate: phosphate antiporter subfamily of major facilitator transporters (Lemieux et al ., 2005; Law et al ., 2009).…”