Depth distributions of alkaline phosphatase and phosphonate utilization genes in the North Pacific Subtropical Gyre

Abstract

The biochemical composition of dissolved organic phosphorus (DOP) in the ocean is dominated by phosphoesters (C-O-P and C-O-P-O-C bonds), which are hydrolyzed by a diverse group of alkaline phosphatases (PhoA, PhoD, PhoX), and by phosphonates (C-P bond), which are degraded by C-P lyases and hydrolases. We designed a bioinformatics pipeline and a statistical approach to recover and analyze the alkaline phosphatase and phosphonate utilization genes from a metagenomic database derived from water samples collected from 7 depths (between 10 and 4000 m) in the oligotrophic North Pacific Subtropical Gyre. The alkaline phosphatase genes phoD and phoX were more abundant than phoA in the euphotic zone (10-130 m) and in deep waters (500-4000 m). The C-P lyase genes were most abundant in the euphotic zone at 70 m and were rare in deep water (≥500 m) where phosphate concentrations were relatively high. These observations indicate that phosphonates are utilized primarily as a phosphorus source by bacterial C-P lyases; this is consistent with the observation that C-P lyase genes are part of the pho regulon which is expressed upon phosphorus limitation. In contrast, C-P hydrolase and alkaline phosphatase genes were often more abundant in deep waters, indicating that DOP serves mainly as a carbon and energy source in phosphaterich deep waters which are depleted in bioavailable dissolved organic matter (DOM). The observed differences in depth distributions and presumed functions of C-P lyase and hydrolase genes indicate variability in the chemical composition of phosphonates between the euphotic zone and deep waters. KEY WORDS: Phosphonate hydrolase · C-P lyase · Alkaline phosphatase · Microbial phosphorus metabolismResale or republication not permitted without written consent of the publisher

Dynamics of Dissolved Organic Phosphorus

“…Each of these APase gene families has unique substrate specificity, metal co-factors and kinetics. Subsequent investigation supported the major ecological role for PhoX, compared to the classical PhoA type of APase (Luo et al, 2011;Sebastian and Ammerman, 2009), in a broad range of marine environments. Since previous APase assay methods were designed to detect primarily periplasmic and outer membrane proteins, and extracellular APase, it is unclear whether the quantitative marine APase database is biased against the more abundant intracellular proteins.…”

Phosphate monoesterase and diesterase activities in the North and South Pacific Ocean

“…Moreover, incubation experiments conducted in the same area showed that the bacterial and primary productions there were not limited by phosphorus Van Wambeke et al, 2008). One explanation for this relatively high MEA coincident with the absence of phosphorus limitation is the deficiency of available organic carbon, based on the hypothesis that another role of alkaline phosphatase in the deep ocean is to decompose the otherwise non-labile dissolved organic matter (Nausch and Nausch, 2004;Luo et al, 2011). Some studies have shown that deficiency of bioavailable organic carbon in the surface water of the subtropical South Pacific is one of the growthlimiting factors of cyanobacteria (Moisander et al, 2012) and heterotrophic bacteria .…”

Organic phosphorus in the aquatic environment

“…[102] Although often assumed to be recalcitrant, recent molecular studies have shown that a diverse range of freshwater and marine bacteria and phytoplankton have genes associated with the production of hydrolytic enzymes capable of catalysing the breakdown of phosphonates. [118][119][120][121] Studies have also shown that phosphonates, particularly glyphosate, can be broken down by Fe-catalysed photolysis, at least in the laboratory. [122] Ecological significance Again, little is known on the ecological significance of phosphonates.…”