Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii.
The marine nitrogen fixing microorganisms (diazotrophs) are a major source of nitrogen to open ocean ecosystems and are predicted to be limited by iron in most marine environments. Here we use global and targeted proteomic analyses on a key unicellular marine diazotroph Crocosphaera watsonii to reveal large scale diel changes in its proteome, including substantial variations in concentrations of iron metalloproteins involved in nitrogen fixation and photosynthesis, as well as nocturnal flavodoxin production. The daily synthesis and degradation of enzymes in coordination with their utilization results in a lowered cellular metalloenzyme inventory that requires ∼40% less iron than if these enzymes were maintained throughout the diel cycle. This strategy is energetically expensive, but appears to serve as an important adaptation for confronting the iron scarcity of the open oceans. A global numerical model of ocean circulation, biogeochemistry and ecosystems suggests that Crocosphaera's ability to reduce its iron-metalloenzyme inventory provides two advantages: It allows Crocosphaera to inhabit regions lower in iron and allows the same iron supply to support higher Crocosphaera biomass and nitrogen fixation than if they did not have this reduced iron requirement.
Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA. msaito@whoi.edu
Mak A
MA
Saito
Erin M
EM
Bertrand
Stephanie
S
Dutkiewicz
Vladimir V
VV
Bulygin
Dawn M
DM
Moran
Fanny M
FM
Monteiro
Michael J
MJ
Follows
Frederica W
FW
Valois
John B
JB
Waterbury
D018533:Biomass; D000458:Cyanobacteria / Q000201:enzymology* / Q000254:growth & development; D005418:Flavodoxin / Q000378:metabolism*; D007501:Iron / Q000378:metabolism*; D008667:Metalloproteins / Q000378:metabolism*; D009586:Nitrogen Fixation / Q000502:physiology*; D009792:Oceans and Seas; D020543:Proteome / Q000378:metabolism*; D012623:Seawater / Q000382:microbiology
D005418:Flavodoxin; D008667:Metalloproteins; D020543:Proteome; D007501:Iron
Chem Rev. 1996 Nov 7;96(7):2965-2982
11848848
Appl Environ Microbiol. 2008 Jul;74(13):4091-100
18469119
Nature. 2004 Aug 26;430(7003):1027-32
15329721
Annu Rev Microbiol. 2008;62:93-111
18429691
Nature. 1997 May 22;387(6631):370-6
9163420
Microbiology (Reading). 1999 Jul;145 ( Pt 7):1749-1758
10439414
Nature. 2001 Aug 9;412(6847):635-8
11493920
Appl Environ Microbiol. 2006 Apr;72(4):2918-24
16597998
Science. 2008 Nov 14;322(5904):1110-2
19008448
Proc Natl Acad Sci U S A. 2009 Apr 14;106(15):6345-50
19332780
Environ Microbiol. 2007 Dec;9(12):2945-56
17991025
Environ Microbiol. 2010 Feb;12(2):412-21
19840103
ISME J. 2009 Jan;3(1):93-105
18769456
Environ Microbiol. 2010 Jan;12(1):54-62
19691503
Science. 2010 Feb 5;327(5966):676-9
20075213
J Bacteriol. 1994 Mar;176(6):1586-97
8132452
Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):6156-61
18427117
Nature. 2004 May 20;429(6989):292-4
15152251
Science. 2005 Jun 24;308(5730):1915-20
15879173
Environ Microbiol. 2009 Feb;11(2):338-48
19196268
Science. 2010 Mar 19;327(5972):1512-4
20185682
Appl Environ Microbiol. 2005 Sep;71(9):5362-70
16151126
Proc Natl Acad Sci U S A. 2006 Feb 14;103(7):2398-403
16467157
Nature. 2009 Aug 6;460(7256):762-5
19606093
Science. 2007 Mar 30;315(5820):1843-6
17395828
Mol Cell Proteomics. 2006 May;5(5):868-81
16489187
J Bacteriol. 2008 Jun;190(11):3904-13
18390663
ISME J. 2010 May;4(5):621-32
20107492
J Proteome Res. 2003 Jan-Feb;2(1):43-50
12643542