The potential for polyphosphate metabolism in Archaea and anaerobic polyphosphate formation in Methanosarcina mazei

Fabiana S Paula,Florence Abram,Anna Schnürer,Katrina A Macintosh,Vincent O’Flaherty,John W Mcgrath,Jasmine Connolly,Jason P Chin,Bettina Müller,John P Quinn,Panagiotis Manesiotis,Nicholas Waters

doi:10.1038/s41598-019-53168-4

Abstract

Inorganic polyphosphate (polyP) is ubiquitous across all forms of life, but the study of its metabolism has been mainly confined to bacteria and yeasts. Few reports detail the presence and accumulation of polyP in Archaea, and little information is available on its functions and regulation. Here, we report that homologs of bacterial polyP metabolism proteins are present across the major taxa in the Archaea, suggesting that archaeal populations may have a greater contribution to global phosphorus cycling than has previously been recognised. We also demonstrate that polyP accumulation can be induced under strictly anaerobic conditions, in response to changes in phosphate (Pi) availability, i.e. Pi starvation, followed by incubation in Pi replete media (overplus), in cells of the methanogenic archaeon Methanosarcina mazei. Pi-starved M. mazei cells increased transcript abundance of the alkaline phosphatase (phoA) gene and of the high-affinity phosphate transport (pstSCAB-phoU) operon: no increase in polyphosphate kinase 1 (ppk1) transcript abundance was observed. Subsequent incubation of Pi-starved M. mazei cells under Pi replete conditions, led to a 237% increase in intracellular polyphosphate content and a > 5.7-fold increase in ppk1 gene transcripts. Ppk1 expression in M. mazei thus appears not to be under classical phosphate starvation control.

Highlights

Polyphosphate consists of a linear chain of orthophosphate (Pi) residues linked together by phosphoanhydride bonds ranging in length from 3 to greater than 1000 residues[1,2]
Searching the National Center for Biotechnology Information (NCBI) RefSeq database for the known enzymes involved in polyP turnover found 442 putative polyphosphate kinase 1 (PPK1), PPK2 and PPX homologs from diverse taxa across the Archaea Domain, it remains to be determined whether these homologs have activity
Whilst putative PPK1 homologs were detected in diverse members of the class Halobacteria and PPK2 homologs in the order Haloferacales, no PPX homologs were found across the class Halobacteria

Summary

Introduction

Polyphosphate (polyP) consists of a linear chain of orthophosphate (Pi) residues linked together by phosphoanhydride bonds ranging in length from 3 to greater than 1000 residues[1,2] It is one of the most widely distributed natural biopolymers, having been detected in many bacteria, fungi, yeasts, plants and animals (reviewed in[3]). Despite this ubiquity, polyP metabolism in both the Archaea and Eukaryotes has received scant attention with the majority of studies focussing on bacterial polyP metabolism. A further understanding of the distribution and regulation of polyP turnover in archaea will provide insights into the ability of these microorganisms to tolerate extreme conditions but will extend our understanding of P cycling in low redox natural and engineered environments

Methods

Results

Conclusion