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Denitrifying and nitrous oxide reducing genotypes

ecophysiology and niche differentiation

Wittorf, Lea (2017). Denitrifying and nitrous oxide reducing genotypes. Diss. (sammanfattning/summary) Uppsala : Sveriges lantbruksuniv., Acta Universitatis agriculturae Sueciae, 1652-6880 ; 2017:98
ISBN 978-91-7760-086-2
eISBN 978-91-7760-087-9
[Doctoral thesis]

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Abstract

Denitrification is a biogeochemical process of major importance for nitrogen loss from
ecosystems. This four-step pathway is modular, as organisms can have different subsets
and variants of the genes involved in each step. The last step is the only known biological
sink of nitrous oxide, a potent greenhouse gas and ozone depleting substance. The aim
of this thesis was to assess whether specific environmental conditions favour certain
denitrifying and nitrous oxide reducing genotypes. The effects of nitrogen, carbon and
oxygen availabilities, as well as habitat type and diversity were examined in studies of
denitrifying and nitrous oxide reducing microorganisms in pure cultures, enrichment
cultures and natural communities from coastal sediments. By utilizing molecular
techniques and directly targeting functional genes encoding for nitrite and nitrous oxide
reductases, this work explores the link between genetic potential and functionality of
denitrifying and nitrous oxide reducing microbial communities.

Microorganisms harbouring genes for complete denitrification dominated in coastal
marine sediments, irrespective of oxygen regime and habitat type, which suggests they
have an important role not only for nitrogen removal, but also nitrous oxide reduction in
coastal ecosystems. However, oxygen affected the nitrous oxide reducing communities.
The results indicate niche differentiation between nitrous oxide reducers in relation to
oxic/anoxic conditions, as specific lineages within the nitrous oxide reductase gene
phylogeny were favoured by certain oxygen regimes. In enrichment cultures, complete
denitrifiers were competitive nitrous oxide reducers and could outcompete organisms
only capable of nitrous oxide reduction when subjected to carbon and nitrous oxide
limitation. For denitrifiers, functional difference between the genes nirS and nirK
encoding two structurally different nitrite reductases within the same organism was
observed, corroborating that closely related and almost identical genotypes differ in their
denitrification activity. Furthermore, primers targeting nitrite reducing communities
harbouring either nirS or nirK were re-evaluated and clade-specific primers are
suggested. Finally, a framework for primer evaluation using metagenomes is suggested.

These results highlight the importance of accounting for the genetic potential of
denitrifying and nitrous oxide reducing communities to better understand overall
ecosystem constraints and how environmental factors might control this potential.

Authors/Creators:Wittorf, Lea
Title:Denitrifying and nitrous oxide reducing genotypes
Subtitle:ecophysiology and niche differentiation
Alternative abstract:
LanguageAbstract
Swedish

Denitrifikation är en biogeokemisk process som har stor betydelse för kväveförlust från
ekosystem. Processen består av fyra steg och är modulär; organismer kan ha genetisk
potential för att utföra alla steg eller enbart vissa av stegen och i varje steg finns det
varianter av generna. Det sista steget är den enda kända biologiska sänkan av
dikväveoxid (lustgas), en potent växthusgas och ozonförstörande substans. Syftet med
denna avhandling var att bedöma om specifika miljöförhållanden gynnar vissa
denitrifierande och lustgasreducerande genotyper. Effekterna av kväve-, kol- och
syretillgänglighet samt av habitattyp och diversitet undersöktes i studier av
denitrifierande och lustgasreducerande mikroorganismer i renkulturer,
anrikningskulturer och i naturliga samhällen från kustsediment. Detta arbete undersöker
sambandet mellan genetisk potential och funktionalitet hos denitrifierande och
lustgasreducerande mikrobiella samhällen genom att använda molekylära tekniker där
funktionella gener som kodar för nitrit- och dikväveoxid-reduktaser utgör målet.

Mikroorganismer som har gener för fullständig denitrifikation dominerade i kustnära
sediment, oberoende av syreförhållanden och habitattyp, vilket tyder på att de har en
viktig roll inte bara för att ta bort kväve, utan också för att reducera lustgas i
kustekosystem. Syre påverkade emellertid de lustgasreducerande samhällena. Resultaten
indikerar att det förekommer nischdifferentiering mellan lustgasreducerande
mikroorganismer i förhållande till oxiska/anoxiska betingelser, eftersom vissa
syreregimer gynnade specifika fylogenetiska linjer av dikväveoxidreduktaser. I
anrikningskulturer var kompletta denitrifierare konkurrenskraftiga och kunde konkurrera
ut lustgasreducerande organismer när kol och lustgas var begränsande. För denitrifierare
observerades funktionell skillnad mellan generna nirS och nirK som kodar för två
strukturellt olika nitritreduktaser i samma organism, vilket bekräftar att även nära
besläktade och nästan identiska genotyper skiljer sig åt i denitrifikationsaktivitet. Vidare
utvärderades primrar för nitritreducerande samhällen, nirS- och nirK-primrar, och
gruppspecifika primrar föreslås. Slutligen föreslås ett ramverk för primerutvärdering med
hjälp av metagenom.

Resultaten i avhandlingen lyfter fram vikten av att räkna med den genetiska
potentialen hos denitrifierande och lustgasreducerande mikrobiella samhällen för att
bättre förstå övergripande ekosystembegränsningar och hur miljöfaktorer kan kontrollera
denna potential.

Series/Journal:Acta Universitatis agriculturae Sueciae (1652-6880)
Year of publishing :2017
Depositing date:2 November 2017
Volume:2017:98
Number of Pages:69
Papers/manuscripts:
NumberReferences
IConthe M, Wittorf L, Kuenen JG, Kleerebezem R, van Loosdrecht MCM,Hallin S. Life on N2O: deciphering the ecophysiology of N2O respiring bacterial communities in a continuous culture. (submitted manuscript)
IIWittorf L, Bonilla-Rosso G, Jones CM, Bäckman O, Hulth S, Hallin S (2016). Habitat partitioning of marine benthic denitrifier communities in response to oxygen availability. Environmental Microbiology Reports 8 (4), 486-492. Corrigendum: Wittorf L, Bonilla-Rosso G, Jones CM, Bäckman O, Hulth S, Hallin S (2016). Habitat partitioning of marine benthic denitrifier communities in response to oxygen availability. Environmental Microbiology Reports 8 (5), 936-936
IIIWittorf L, Roger F, Alsterberg C, Gamfeldt L, Sundbäck K, Hulth S, Jones CM, Hallin S. Ecosystem complexity shapes nitrous oxide reducing and denitrifying communities in coastal sediments. (submitted manuscript)
IVWittorf L, Jones CM, Bonilla-Rosso G, Hallin S. Expression of nirK and nirS genes encoding structurally distinct NO-forming nitrite reductases within the same strain of Pseudomonas stutzeri. (manuscript)
VBonilla-Rosso G, Wittorf L, Jones CM, Hallin S (2016). Design and evaluation of primers targeting genes encoding NO-forming nitrite reductases: implications for ecological inference of denitrifying communities. Scientific Reports 6 (39208).
Place of Publication:Uppsala
Publisher:Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences
ISBN for printed version:978-91-7760-086-2
ISBN for electronic version:978-91-7760-087-9
ISSN:1652-6880
Language:English
Publication Type:Doctoral thesis
Full Text Status:Public
Agris subject categories.:P Natural resources > P01 Nature conservation and land resources
P Natural resources > P34 Soil biology
T Pollution > T01 Pollution
X Agricola extesions > X30 Life sciences
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 105 Earth and Related Environmental Sciences > Environmental Sciences (social aspects to be 507)
(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Biochemistry and Molecular Biology
(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Microbiology (Microbiology in the medical area to be 30109)
(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Bioinformatics and Systems Biology (methods development to be 10203)
(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Ecology
Agrovoc terms:denitrification, microorganisms, oxidoreductases, redox potential, nitrous oxide, genotypes, gene expression, coastal soils
Keywords:Denitrifying microorganisms, nitrous oxide reducers, genetic potential, nirK, nirS, nosZ, marine sediment, gene expression, enrichment, diversity
URN:NBN:urn:nbn:se:slu:epsilon-e-4448
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-e-4448
ID Code:14682
Faculty:NJ - Fakulteten för naturresurser och jordbruksvetenskap
Department:(NL, NJ) > Dept. of Forest Mycology and Plant Pathology
(S) > Dept. of Forest Mycology and Plant Pathology
External funders:Swedish Research Council
Deposited By: Lea Wittorf
Deposited On:03 Nov 2017 10:00
Metadata Last Modified:03 Nov 2017 10:00

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