Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic alpine lakes.
The annual changes in the composition and abundance of ammonia-oxidizing archaea (AOA) were analyzed monthly in surface waters of three high mountain lakes within the Limnological Observatory of the Pyrenees (LOOP; northeast Spain) using both 16S rRNA and functional (ammonia monooxygenase gene, amoA) gene sequencing as well as quantitative PCR amplification. The set of biological data was related to changes in nitrogen species and to other relevant environmental variables. The whole archaeal assemblage was dominated by phylotypes closely related to the crenarchaeal 1.1a group (58% ± 18% of total 16S rRNA gene sequences), and consistent structural changes were detected during the study. Water temperature was the environmental variable that better explained spring, summer, and winter (ice-covered lakes) archaeal assemblage structure. The amoA gene was detected year round, and seasonal changes in amoA gene composition were well correlated with changes in the archaeal 16S rRNA gene pool. In addition, copy numbers of both the specific 1.1a group 16 rRNA and archaeal amoA genes were well correlated, suggesting that most freshwater 1.1a Crenarchaeota had the potential to carry out ammonia oxidation. Seasonal changes in the diversity and abundance of AOA (i.e., amoA) were better explained by temporal changes in ammonium, the substrate for nitrification, and mostly nitrite, the product of ammonia oxidation. Lacustrine amoA gene sequences grouped in coherent freshwater phylogenetic clusters, suggesting that freshwater habitats harbor typical amoA-containing ecotypes, which is different from soils and seas. We observed within the freshwater amoA gene sequence pool a high genetic divergence (translating to up to 32% amino acid divergence) between the spring and the remaining AOA assemblages. This suggests that different AOA ecotypes are adapted to different temporal ecological niches in these lakes.
Centro de Estudios Avanzados de Blanes, CEAB-CSIC, Accés Cala Sant Francesc 14, E-17300, Blanes, Spain. jcauguet@ceab.csic.es
Jean-Christophe
JC
Auguet
Natalya
N
Nomokonova
Lluis
L
Camarero
Emilio O
EO
Casamayor
D000641:Ammonia / Q000378:metabolism*; D001105:Archaea / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D044822:Biodiversity; D005618:Fresh Water; D008969:Molecular Sequence Data; D009584:Nitrogen / Q000378:metabolism*; D010088:Oxidoreductases / Q000235:genetics; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D012621:Seasons; D013030:Spain
D012336:RNA, Ribosomal, 16S; D000641:Ammonia; D010088:Oxidoreductases; C045582:ammonia monooxygenase; D009584:Nitrogen
Environ Microbiol. 2008 Nov;10(11):3002-16
18973621
FEMS Microbiol Ecol. 2007 Dec;62(3):242-57
17991018
ISME J. 2008 Apr;2(4):429-41
18200070
Environ Microbiol. 2010 Mar;12(3):679-88
20002133
Environ Microbiol. 2009 Mar;11(3):687-99
19207564
Nature. 2005 Sep 22;437(7058):543-6
16177789
Nature. 2009 Oct 15;461(7266):976-9
19794413
Am Nat. 2007 Mar;169(3):E68-83
17230400
Appl Environ Microbiol. 2010 Apr;76(8):2517-23
20190081
Proc Natl Acad Sci U S A. 2005 Oct 11;102(41):14683-8
16186488
Environ Microbiol. 2008 Apr;10(4):1080-6
18215160
Bioinformatics. 2006 Jul 1;22(13):1658-9
16731699
Methods Mol Biol. 2009;537:39-64
19378139
Environ Microbiol. 2007 Sep;9(9):2364-74
17686032
Mol Biol Evol. 2000 Apr;17(4):540-52
10742046
Syst Biol. 2008 Oct;57(5):758-71
18853362
Science. 2004 Apr 2;304(5667):66-74
15001713
Appl Environ Microbiol. 2004 Apr;70(4):2404-13
15066838
Appl Microbiol Biotechnol. 2004 Jun;64(5):726-34
14997354
Nature. 2006 Aug 17;442(7104):806-9
16915287
Environ Microbiol. 2005 Dec;7(12):1985-95
16309395
FEMS Microbiol Ecol. 2008 May;64(2):175-86
18336555
Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5685-9
1608980
Nucleic Acids Res. 2004 Feb 25;32(4):1363-71
14985472
Environ Microbiol. 2008 Sep;10(9):2200-10
18637951
Environ Microbiol. 2008 Nov;10(11):2931-41
18973620
Environ Microbiol. 2009 Jun;11(6):1612-23
19453609
Appl Environ Microbiol. 2006 Jul;72(7):5069-72
16820507
BMC Bioinformatics. 2006 Aug 07;7:371
16893466
Appl Environ Microbiol. 1998 Nov;64(11):4299-306
9797280
FEMS Microbiol Rev. 2009 Sep;33(5):855-69
19453522
Appl Environ Microbiol. 2000 Feb;66(2):499-508
10653710
Bioinformatics. 2007 Jan 1;23(1):127-8
17050570
Appl Environ Microbiol. 2009 Jul;75(14):4687-95
19465520
Appl Environ Microbiol. 2010 Oct;76(20):6853-63
20802065
Environ Microbiol. 2008 Nov;10(11):2966-78
18707610
Appl Environ Microbiol. 2009 May;75(10):3127-36
19304820
Environ Microbiol. 2010 Jul;12(7):1989-2006
20345944
Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12317-22
16894176
Appl Environ Microbiol. 1993 Mar;59(3):695-700
7683183
FEMS Microbiol Rev. 2000 Dec;24(5):673-90
11077158
Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7104-9
17420469
BMC Bioinformatics. 2003 Jul 10;4:29
12854978
FEMS Microbiol Ecol. 2008 Nov;66(2):331-42
18754782
ISME J. 2010 Feb;4(2):182-90
19847207
Appl Environ Microbiol. 2002 Oct;68(10):4751-7
12324316
Appl Environ Microbiol. 2002 Jun;68(6):3094-101
12039771
Environ Microbiol. 2008 Jun;10(6):1601-11
18336563
J Mol Biol. 1990 Oct 5;215(3):403-10
2231712
ISME J. 2007 May;1(1):19-27
18043610
Environ Microbiol. 2010 May;12(5):1282-92
20192962