title: Microbial tailoring of acyl peptidic siderophores.
abstract: Marine bacteria produce an abundance of suites of acylated siderophores characterized by a unique, species-dependent headgroup that binds iron(III) and one of a series of fatty acid appendages. Marinobacter sp. DS40M6 produces a suite of seven acylated marinobactins, with fatty acids ranging from saturated and unsaturated C12-C18 fatty acids. In the present study, we report that in the late log phase of growth, the fatty acids are hydrolyzed by an amide hydrolase producing the peptidic marinobactin headgroup. Halomonas aquamarina str. DS40M3, another marine bacterium isolated originally from the same sample of open ocean water as Marinobacter sp. DS40M6, produces the acyl aquachelins, also as a suite composed of a peptidic headgroup distinct from that of the marinobactins. In contrast to the acyl marinobactins, hydrolysis of the suite of acyl aquachelins is not detected, even when H. aquamarina str. DS40M3 is grown into the stationary phase. The Marinobacter cell-free extract containing the acyl amide hydrolase is active toward exogenous acyl-peptidic siderophores (e.g., aquachelin C, loihichelin C, as well as octanoyl homoserine lactone used in quorum sensing). Further, when H. aquamarina str. DS40M3 is cultured together with Marinobacter sp. DS40M6, the fatty acids of both suites of siderophores are hydrolyzed, and the aquachelin headgroup is also produced. The present study demonstrates that coculturing bacteria leads to metabolically tailored metabolites compared to growth in a single pure culture, which is interesting given the importance of siderophore-mediated iron acquisition for bacterial growth and that Marinobacter sp. DS40M6 and H. aquamarina str. DS40M3 were isolated from the same sample of seawater.
authors.affiliation: Department of Chemistry and Biochemistry, University of California , Santa Barbara, California 93106-9510, United States.
authors.forename: Julia M
authors.initials: JM
authors.lastname: Gauglitz
authors.forename: Akira
authors.initials: A
authors.lastname: Iinishi
authors.forename: Yusai
authors.initials: Y
authors.lastname: Ito
authors.forename: Alison
authors.initials: A
authors.lastname: Butler
mesh_terms: D000581:Amidohydrolases / Q000378:metabolism; D001431:Bacteriological Techniques / Q000379:methods; D002474:Cell-Free System; D018920:Coculture Techniques; D020632:Halomonas / Q000254:growth & development / Q000378:metabolism*; D006868:Hydrolysis; D009682:Magnetic Resonance Spectroscopy; D053520:Marinobacter / Q000378:metabolism; D015394:Molecular Structure; D009842:Oligopeptides / Q000737:chemistry / Q000378:metabolism; D010169:Palmitic Acids / Q000737:chemistry / Q000378:metabolism; D010455:Peptides / Q000737:chemistry / Q000378:metabolism; D010456:Peptides, Cyclic / Q000737:chemistry / Q000378:metabolism; D017262:Siderophores / Q000737:chemistry* / Q000378:metabolism*; D013997:Time Factors; D000099252:Fatty Acid Amide Hydrolases
chemical_list: D000581:Amidohydrolases; D009842:Oligopeptides; D010169:Palmitic Acids; D010455:Peptides; D010456:Peptides, Cyclic; D017262:Siderophores; D000099252:Fatty Acid Amide Hydrolases; C547048:aquachelin-C; C000590833:loihichelin C; C000590834:marinobactin A; C521124:marinobactin E
references.citation: Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):3754-9
references.pmid: 12651947
references.citation: Amino Acids. 2010 May;38(5):1447-59
references.pmid: 19787431
references.citation: J Mol Biol. 2008 Dec 5;384(1):193-205
references.pmid: 18824174
references.citation: Proc Natl Acad Sci U S A. 2010 Jan 12;107(2):686-91
references.pmid: 20080736
references.citation: J Inorg Biochem. 2012 Feb;107(1):90-5
references.pmid: 22178670
references.citation: J Am Chem Soc. 2012 Mar 21;134(11):5415-22
references.pmid: 22381697
references.citation: Tuberculosis (Edinb). 2004;84(1-2):110-30
references.pmid: 14670352
references.citation: Biomed Mass Spectrom. 1984 Nov;11(11):601
references.pmid: 6525415
references.citation: Biometals. 1995 Oct;8(4):309-17
references.pmid: 7580051
references.citation: Org Biomol Chem. 2012 Dec 21;10(47):9338-43
references.pmid: 22972004
references.citation: Environ Microbiol Rep. 2010 Jun;2(3):419-25
references.pmid: 23766115
references.citation: Environ Microbiol. 2013 Mar;15(3):916-27
references.pmid: 23320867
references.citation: J Am Chem Soc. 2005 Feb 16;127(6):1726-36
references.pmid: 15701007
references.citation: Science. 2000 Feb 18;287(5456):1245-7
references.pmid: 10678827
references.citation: FEBS Lett. 2012 Jan 2;586(1):96-101
references.pmid: 22172280
references.citation: J Nat Prod. 2009 May 22;72(5):884-8
references.pmid: 19320498
references.citation: Environ Microbiol. 2012 Aug;14(8):1982-94
references.pmid: 22498339
references.citation: Chem Rev. 2009 Oct;109(10):4580-95
references.pmid: 19772347
references.citation: J Biol Chem. 2007 Jul 13;282(28):20425-34
references.pmid: 17502378
references.citation: J Bacteriol. 2006 Jan;188(2):424-30
references.pmid: 16385031
references.citation: J Inorg Biochem. 2007 Nov;101(11-12):1692-8
references.pmid: 17868890
references.citation: ACS Chem Biol. 2011 Nov 18;6(11):1277-86
references.pmid: 21892836
references.citation: J Am Chem Soc. 2002 Nov 13;124(45):13408-15
references.pmid: 12418892
references.citation: J Biol Inorg Chem. 2006 Jul;11(5):633-41
references.pmid: 16791646
references.citation: Anal Biochem. 1987 Jan;160(1):47-56
references.pmid: 2952030
references.citation: J Exp Med. 1996 Apr 1;183(4):1527-32
references.pmid: 8666910
references.citation: Biometals. 1993 Summer;6(2):93-100
references.pmid: 7689374
references.citation: J Biol Inorg Chem. 2013 Jun;18(5):489-97
references.pmid: 23564034
references.citation: Annu Rev Microbiol. 2000;54:881-941
references.pmid: 11018148
references.citation: Environ Microbiol. 2013 Jun;15(6):1661-73
references.pmid: 23126435
references.citation: Biometals. 2011 Feb;24(1):85-92
references.pmid: 20853137
references.citation: Nat Chem Biol. 2005 Aug;1(3):149-53
references.pmid: 16408019
references.citation: FEBS Lett. 2010 Dec 1;584(23):4751-5
references.pmid: 21035449