Bacterial catabolism of membrane phospholipids links marine biogeochemical cycles

Author:

Westermann Linda M.1ORCID,Lidbury Ian D. E. A.2ORCID,Li Chun-Yang3ORCID,Wang Ning4ORCID,Murphy Andrew R. J.1ORCID,Aguilo Ferretjans Maria del Mar1ORCID,Quareshy Mussa1ORCID,Shanmugan Muralidharan5ORCID,Torcello-Requena Alberto1ORCID,Silvano Eleonora1ORCID,Zhang Yu-Zhong34ORCID,Blindauer Claudia A.6ORCID,Chen Yin1ORCID,Scanlan David J.1ORCID

Affiliation:

1. School of Life Sciences, University of Warwick, Gibbet Hill Road, Coventry, CV4 7AL, UK.

2. Molecular Microbiology: Biochemistry to Disease, School of Biosciences, University of Sheffield, Sheffield, S10 2TN, UK.

3. College of Marine Life Sciences and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China.

4. State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China.

5. Department of Chemistry and Photon Science Institute, The University of Manchester, Oxford Road, Manchester, M13 9PL, UK.

6. Department of Chemistry, University of Warwick, Coventry, CV4 7AL, UK.

Abstract

In marine systems, the availability of inorganic phosphate can limit primary production leading to bacterial and phytoplankton utilization of the plethora of organic forms available. Among these are phospholipids that form the lipid bilayer of all cells as well as released extracellular vesicles. However, information on phospholipid degradation is almost nonexistent despite their relevance for biogeochemical cycling. Here, we identify complete catabolic pathways for the degradation of the common phospholipid headgroups phosphocholine (PC) and phosphorylethanolamine (PE) in marine bacteria. Using Phaeobacter sp. MED193 as a model, we provide genetic and biochemical evidence that extracellular hydrolysis of phospholipids liberates the nitrogen-containing substrates ethanolamine and choline. Transporters for ethanolamine (EtoX) and choline (BetT) are ubiquitous and highly expressed in the global ocean throughout the water column, highlighting the importance of phospholipid and especially PE catabolism in situ. Thus, catabolic activation of the ethanolamine and choline degradation pathways, subsequent to phospholipid metabolism, specifically links, and hence unites, the phosphorus, nitrogen, and carbon cycles.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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