Lipid remodelling is a widespread strategy in marine heterotrophic bacteria upon phosphorus deficiency

Abstract

Upon phosphorus (P) deficiency, marine phytoplankton reduce their requirements for P by replacing membrane phospholipids with alternative non-phosphorus lipids. It was very recently demonstrated that a SAR11 isolate also shares this capability when phosphate starved in culture. Yet, the extent to which this process occurs in other marine heterotrophic bacteria and in the natural environment is unknown. Here, we demonstrate that the substitution of membrane phospholipids for a variety of non-phosphorus lipids is a conserved response to P deficiency among phylogenetically diverse marine heterotrophic bacteria, including members of the Alphaproteobacteria and Flavobacteria. By deletion mutagenesis and complementation in the model marine bacterium Phaeobacter sp. MED193 and heterologous expression in recombinant Escherichia coli, we confirm the roles of a phospholipase C (PlcP) and a glycosyltransferase in lipid remodelling. Analyses of the Global Ocean Sampling and Tara Oceans metagenome data sets demonstrate that PlcP is particularly abundant in areas characterized by low phosphate concentrations. Furthermore, we show that lipid remodelling occurs seasonally and responds to changing nutrient conditions in natural microbial communities from the Mediterranean Sea. Together, our results point to the key role of lipid substitution as an adaptive strategy enabling heterotrophic bacteria to thrive in the vast P-depleted areas of the ocean.

Planktonic Lipidome Responses to Aeolian Dust Input in Low-Biomass Oligotrophic Marine Mesocosms

“…the shared feature of short and saturated alkyl chains is consistent with the production of PC, DGTS, DGTA, DGDG, SQ, and MGDG.3 by heterotrophic bacteria in the oligotrophic EMS, who may thus adjust these IPLs in response to nutrient availability via mechanisms previously described for eukaryotes and cyanobacteria ) and hetertrophic bacteria (Sebastián et al, 2016). MGDG-OH, MGDG+H 2 O, AA-L.1, and AA-L.2 lipids comprised ≤4 compounds and therefore were not included in the clustering analysis.…”

“…However, in this study, IPLs that have been associated with nutrientavailability (i.e., PC, SQ, and betaine lipids; Van Mooy et al, 2009; Table 4) were relatively enriched in short (i.e., sum ≤ C 34 ) and saturated alkyl chains (Figure 5), which is a feature that appears to distinguish this cluster from the major glycolipids and is generally attributed to heterotrophic bacteria (e.g., Kaneda, 1991;Thompson, 1996;Bergé and Barnathan, 2005). This finding is consistent with Sebastián et al (2016), who suggested that heterotrophic bacteria remodel their cell membrane in response to nutrient availability, increasing levels of DGTS during Pdeficiency and increasing levels of PC when P becomes available.…”

“…Biogeochemical responses to the addition of SD or A, including plankton community composition and production, pigment concentration, and cycling of macro-nutrients and trace elements, were compared in triplicate to unamended control mesocosms over a period of 8 days (Guo et al, 2016;Herut et al, 2016;Rahav et al, 2016;Tsiola et al, 2016;Tsagaraki et al, under revision, this SI). In addition to these bulk biogeochemical measures of food web dynamics, the diversity of algal and bacterial cell membrane lipids provides a moderate level of taxonomic and physiological information (e.g., Sato, 1992;Guschina and Harwood, 2006;Sohlenkamp and Geiger, 2015) that can be applied to assess organic matter reactivity (Harvey and Macko, 1997;Wakeham et al, 1997), plankton communities in the ocean (e.g., Van Mooy and Fredricks, 2010), and carbon and nutrient fluxes in marine food webs (Dalsgaard et al, 2003;Sebastián et al, 2016). For example, phytoplankton populations are able to reduce their cellular P quota by substituting phospholipids with sulfolipids or betaine lipids when P is limiting ) and nutrient gradients across the Mediterranean appear to drive the lipid distribution of plankton communities (Popendorf et al, 2011b).…”

“…One subgroup comprised only glycolipids and the other comprised PC, DGTA, DGTS, and SQ, which are modulated by eukaryotes and cyanobacteria ) as well as heterotrophic bacteria (Sebastián et al, 2016) in response to nutrient availability.…”

Comparative genomic, proteomic and exoproteomic analyses of three Pseudomonas strains reveals novel insights into the phosphorus scavenging capabilities of soil bacteria

“…A total of 267 proteins were significantly enriched [ t ‐test, P value ≤ 0.05, fold‐change (log2) ≥ 1.5] during Pi depletion and there was concordance between the two datasets. These enriched proteins included the transmembrane and ATP‐binding domains of the Pst system (PstC, PstA, PstB), a 2‐aminoethylphosphonate (2‐AEP)–specific phosphonatase (PhnX, PhnW) (Jiang et al ., 1995; Baker et al ., 1998; White and Metcalf, 2007), proteins involved in lipid remodelling (PlcP, DagK, OlsA, OlsB, Cfa, TauD) (Liu and Hulett, 1998; Antelmann et al ., 2000; Zavaleta‐Pastor et al ., 2010; Carini et al ., 2015; Sebastian et al ., 2016), a putative intracellular phosphatase (UxpA) and the twin‐arginine translocation (TAT) pathway (Putker et al ., 2013) (Table 2). Proteins for both starch (MalQ, GlgE, GlgX, GlpA and GlpB) and polyhydroxyalkanoic acid (PhaA, PhaG, PhaC) biosynthesis (carbon storage) were also enriched during Pi stress (Supporting Information Table S4).…”