Circumventing kinetics in biogeochemical modeling.
geobiology
marine anoxic region
microbial system
reaction kinetics
redox gradient
Journal
Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876
Informations de publication
Date de publication:
04 06 2019
04 06 2019
Historique:
pubmed:
18
5
2019
medline:
24
3
2020
entrez:
18
5
2019
Statut:
ppublish
Résumé
Microbial metabolism drives biogeochemical fluxes in virtually every ecosystem. Modeling these fluxes is challenged by the incredible diversity of microorganisms, whose kinetic parameters are largely unknown. In poorly mixed systems, such as stagnant water columns or sediments, however, long-term bulk microbial metabolism may become limited by physical transport rates of substrates across space. Here we mathematically show that under these conditions, biogeochemical fluxes are largely predictable based on the system's transport properties, chemical boundary conditions, and the stoichiometry of metabolic pathways, regardless of the precise kinetics of the resident microorganisms. We formalize these considerations into a predictive modeling framework and demonstrate its use for the Cariaco Basin subeuphotic zone, one of the largest anoxic marine basins worldwide. Using chemical concentration data solely from the upper boundary (depth 180 m) and lower boundary (depth 900 m), but without a priori knowledge of metabolite fluxes, chemical depth profiles, kinetic parameters, or microbial species composition, we predict the concentrations and vertical fluxes of biologically important substances, including oxygen, nitrate, hydrogen sulfide, and ammonium, across the entire considered depth range (180-900 m). Our predictions largely agree with concentration measurements over a period of 14 years ([Formula: see text] = 0.78-0.92) and become particularly accurate during a period where the system was near biogeochemical steady state (years 2007-2009, [Formula: see text] = 0.86-0.95). Our work enables geobiological predictions for a large class of ecosystems without knowledge of kinetic parameters or geochemical depth profiles. Conceptually, our work provides a possible explanation for the decoupling between microbial species composition and bulk metabolic function, observed in various ecosystems.
Identifiants
pubmed: 31097587
pii: 1819883116
doi: 10.1073/pnas.1819883116
pmc: PMC6561284
doi:
Substances chimiques
Ammonium Compounds
0
Nitrates
0
Oxygen
S88TT14065
Hydrogen Sulfide
YY9FVM7NSN
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
11329-11338Déclaration de conflit d'intérêts
The authors declare no conflict of interest.
Références
Nat Rev Microbiol. 2012 May 14;10(6):381-94
pubmed: 22580367
Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):E5925-E5933
pubmed: 27655888
Appl Environ Microbiol. 2001 Apr;67(4):1663-74
pubmed: 11282619
Nat Commun. 2018 Jul 16;9(1):2743
pubmed: 30013041
Wiley Interdiscip Rev Syst Biol Med. 2010 May-Jun;2(3):372-382
pubmed: 20836035
Nat Rev Microbiol. 2008 Mar;6(3):199-210
pubmed: 18264116
Science. 2014 Nov 7;346(6210):735-9
pubmed: 25378621
Monogr Popul Biol. 1982;17:1-296
pubmed: 7162524
J Contam Hydrol. 2001 Feb;47(2-4):297-309
pubmed: 11288584
FEMS Microbiol Ecol. 2015 Sep;91(9):fiv088
pubmed: 26209697
Appl Environ Microbiol. 2007 Jan;73(2):451-5
pubmed: 17114324
ISME J. 2018 Jan;12(1):1-16
pubmed: 29099490
Proc Natl Acad Sci U S A. 2016 Sep 20;113(38):10601-6
pubmed: 27601665
Proc Natl Acad Sci U S A. 2012 Nov 20;109(47):19315-20
pubmed: 23071299
Nat Ecol Evol. 2018 Jun;2(6):936-943
pubmed: 29662222
Nat Ecol Evol. 2016 Dec 05;1(1):15
pubmed: 28812567
Geobiology. 2009 Sep;7(4):385-92
pubmed: 19702823
Science. 2018 Jan 5;359(6371):
pubmed: 29301986
Nature. 2009 Jan 22;457(7228):480-4
pubmed: 19043404
Microb Ecol. 2015 Oct;70(3):596-611
pubmed: 25912922
Ann Rev Mar Sci. 2019 Jan 3;11:413-437
pubmed: 29889611
Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):15996-6003
pubmed: 22967509
FEMS Microbiol Ecol. 2007 Jun;60(3):351-7
pubmed: 17524119
Science. 2016 Sep 16;353(6305):1272-7
pubmed: 27634532
Geobiology. 2019 Nov;17(6):628-642
pubmed: 31496030
Appl Environ Microbiol. 2008 Dec;74(24):7546-51
pubmed: 18952879
Biochem Soc Trans. 2012 Dec 1;40(6):1315-8
pubmed: 23176474
J Bacteriol. 2003 Mar;185(5):1485-91
pubmed: 12591863
Appl Environ Microbiol. 1999 Aug;65(8):3697-704
pubmed: 10427068
Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7104-9
pubmed: 17420469
mSystems. 2018 Sep 25;3(5):
pubmed: 30273414
Environ Microbiol. 2010 Jan;12(1):172-91
pubmed: 19788414
Appl Environ Microbiol. 2005 Nov;71(11):7389-400
pubmed: 16269781
Biotechnol Bioeng. 2008 Mar 1;99(4):830-45
pubmed: 17705250
Nat Biotechnol. 2010 Mar;28(3):245-8
pubmed: 20212490
Appl Environ Microbiol. 2006 Apr;72(4):2679-90
pubmed: 16597973
Proc Natl Acad Sci U S A. 2014 Feb 4;111(5):1879-84
pubmed: 24449851