System-Wide Adaptations of Desulfovibrio alaskensis G20 to Phosphate-Limited Conditions

Abstract

The prevalence of lipids devoid of phosphorus suggests that the availability of phosphorus limits microbial growth and activity in many anoxic, stratified environments. To better understand the response of anaerobic bacteria to phosphate limitation and starvation, this study combines microscopic and lipid analyses with the measurements of fitness of pooled barcoded transposon mutants of the model sulfate reducing bacterium Desulfovibrio alaskensis G20. Phosphate-limited G20 has lower growth rates and replaces more than 90% of its membrane phospholipids by a mixture of monoglycosyl diacylglycerol (MGDG), glycuronic acid diacylglycerol (GADG) and ornithine lipids, lacks polyphosphate granules, and synthesizes other cellular inclusions. Analyses of pooled and individual mutants reveal the importance of the high-affinity phosphate transport system (the Pst system), PhoR, and glycolipid and ornithine lipid synthases during phosphate limitation. The phosphate-dependent synthesis of MGDG in G20 and the widespread occurrence of the MGDG/GADG synthase among sulfate reducing ∂-Proteobacteria implicate these microbes in the production of abundant MGDG in anaerobic environments where the concentrations of phosphate are lower than 10 μM. Numerous predicted changes in the composition of the cell envelope and systems involved in transport, maintenance of cytoplasmic redox potential, central metabolism and regulatory pathways also suggest an impact of phosphate limitation on the susceptibility of sulfate reducing bacteria to other anthropogenic or environmental stresses.

Influence of Phosphorus and Cell Geometry on the Fractionation of Sulfur Isotopes by Several Species of Desulfovibrio during Microbial Sulfate Reduction

“…Morphological changes observed in the two Desulfovibrio spp. we tested (see below), as well as structural adaptations to phosphate limitation and starvation observed in D. desulfuricans (Weimer et al, 1988) and D. alaskensis G20 (Bosak et al, 2016) are consistent with the higher bulk C:P ratio in phosphate-limited D. desulfuricans (Okabe and Characklis, 1992). …”

Intact polar lipids in the water column of the eastern tropical North Pacific: abundance and structural variety of non-phosphorus lipids

“…Figure 3 shows changes in the relative abundances (as percentages of total IPLs, excluding isoprenoidal archaeal IPLs) of glycolipids, phospholipids and aminolipids as well as several substitute lipid ratios, reflecting the preferential biosynthesis of non-phosphorus lipids to replace phospholipids under phosphate-limiting growth (cf. Van Mooy et al, 2006;Popendorf et al, 2011b;Carini et al, 2015;Bosak et al, 2016). Relative abundances of non-isoprenoidal phospholipids were highest in the core OMZ between 400 and 600 m at all sites, where they comprise up to 45 %-76 % at Stations 1, 2 and 5 and between 12 % and 61 % at Station 8.…”

“…The assignment of the betaine lipid DGTS was according to the retention time of the commercially available standard DGTS (Avanti Polar Lipids, USA). The isomer DGTA, which elutes at a different retention time due to its structural difference (e.g., Brandsma et al, 2012), was not observed in the HPLC-MS chromatograms. For all analyses, response factors of individual IPLs relative to the injection standard C 19 -PC were determined using dilution series of commercially available standards (Table S2).…”

“…IPLs represent a diverse range of molecular structures, including phosphatidyl, glycosidic, phospho-glycosidic, and amino acid polar head groups linked to glyceryl-acyl and glyceryl-O-alkyl apolar moieties. IPL distributions have been documented in surface waters of the eastern subtropical South Pacific (Van Mooy and Fredricks, 2010), the western North Atlantic Ocean (Van Mooy et al, 2006Popendorf et al, 2011a), the South Pacific Ocean (Kharbush et al, 2016), the Mediterranean Sea (Popendorf et al, 2011b), the North Sea (Brandsma et al, 2012), lakes (Bale et al, 2016, the western English Channel (White et al, 2015) and throughout the water columns of stratified water bodies (Ertefai et al, 2008;Schubotz et al, 2009;Wakeham et al, 2012;Pitcher et al, 2011;Xie et al, 2014;Basse et al, 2014;Sollai et al, 2015). Surface waters are typically dominated by nine IPL classes.…”

“…Heterotrophic marine bacteria can replace PE-DAG with either 1G-DAG or DGTS (Carini et al, 2015;Sebastian et al, 2016;Yao et al, 2015). Notably, substitute lipids are also biosynthesized under micromolar concentrations of phosphate (Bosak et al, 2016).…”