Phosphonate utilization by the globally important marine diazotroph Trichodesmium

Abstract

The factors that control the growth and nitrogen fixation rates of marine diazotrophs such as Trichodesmium have been intensively studied because of the role that these processes have in the global cycling of carbon and nitrogen, and in the sequestration of carbon to the deep sea. Because the phosphate concentrations of many ocean gyres are low, the bioavailability of the larger, chemically heterogeneous pool of dissolved organic phosphorus could markedly influence Trichodesmium physiology. Here we describe the induction, by phosphorus stress, of genes from the Trichodesmium erythraeum IMS101 genome that are predicted to encode proteins associated with the high-affinity transport and hydrolysis of phosphonate compounds by a carbon-phosphorus lyase pathway. We show the importance of these genes through expression analyses with T. erythraeum from the Sargasso Sea. Phosphonates are known to be present in oligotrophic marine systems, but have not previously been considered to be bioavailable to marine diazotrophs. The apparent absence of genes encoding a carbon-phosphorus lyase pathway in the other marine cyanobacterial genomes suggests that, relative to other phytoplankton, Trichodesmium is uniquely adapted for scavenging phosphorus from organic sources. This adaptation may help to explain the prevalence of Trichodesmium in low phosphate, oligotrophic systems.

Potential for phosphite and phosphonate utilization by Prochlorococcus

“…Pns bioavailability was suggested to influence markedly bacterial primary production (Karl and Bjö rkman, 2002;Gilbert et al, 2009;Thomas et al, 2010), possibly providing an evolutionary advantage to species able to utilize Pn. The gene encoding the Pn-binding protein (phnD) of the ABC-type Pn transporter is found in genomes of different marine bacteria and is used as one of several proxies for the ability to assimilate Pns in natural microbial assemblages (Dyhrman et al, 2006;Ilikchyan et al, 2009Ilikchyan et al, , 2010.…”

“…The phnD gene is found in numerous marine bacterial genomes, including genomes of the globally abundant marine bacteria Trichodesmium (Dyhrman et al, 2006), Synechococcus, Prochlorococcus and Pelagibacter (the SAR11 group). Enrichment in SAR11 Pn utilization genes or peptides was reported in the P-depleted eastern Mediterranean Sea (via metagenomics (Feingersch et al, 2010)) and the Sargasso Sea (via metaproteomics (Sowell et al, 2009) and metagenomics (Coleman and Chisholm, 2010)), whereas cyanobacterial phnD genes were shown to be expressed in P-deficient media and in the environment (Dyhrman et al, 2006;Ilikchyan et al, 2009Ilikchyan et al, , 2010Beversdorf et al, 2010).…”

Evidence for phosphonate usage in the coral holobiont

“…Phosphonates, which contain a carbon-phosphorus bond, can account for 25% of the dissolved organic phosphorus pool in marine environments (Dyhrman et al, 2006) and for 10% of cellular particulate phosphate in Trichodesmium , and are important in marine microbial populations (Benitez-Nelson et al, 2004;Karl et al, 2008;Gilbert et al, 2009;Ilikchyan et al, 2009;Martinez et al, 2009). Phosphonates are, by virtue of the carbon-phosphorus bond, both thermally and hydrolytically stable, and form lipid and protein conjugates widely distributed in the Cnidaria (Hilderbrand, 1983).…”

Introduction to the special issue: Developments in soil organic phosphorus cycling in natural and agricultural ecosystems

“…This work has been conducted primarily in marine environments (e.g. Dyhrman et al, 2006), with little application in terrestrial or freshwater ecosystems. However, an article in the special issue reports that the bacterial gene for alkaline phosphomonoesterase activity (phoD) has been examined in soils of a long-term management trial in Canada (Fraser et al, 2015).…”