Freshwater bacteria release methane as a byproduct of phosphorus acquisition.
Freshwater lakes emit large amounts of methane, some of which is produced in oxic surface waters. Two potential pathways for aerobic methane production exist: methanogenesis in oxygenated water, which has been observed in some lakes, or demethylation of small organic molecules. Although methane is produced via demethylation in oxic marine environments, this mechanism of methane release has not yet been demonstrated in freshwater systems. Genes related to the C-P lyase pathway, which cleaves C-P bonds in phosphonate compounds, were found in a metagenomic survey of the surface water of Lake Matano, which is chronically P-starved and methane-rich. We demonstrate that four bacterial isolates from Lake Matano obtain P from methylphosphonate and release methane, and that this activity is repressed by phosphate. We further demonstrate that expression of phnJ, which encodes the enzyme that releases methane, is higher in the presence of methylphosphonate and lower when both methylphosphonate and phosphate are added. This gene is also found in most of the metagenomic data sets from freshwater environments. These experiments link methylphosphonate degradation and methane production with gene expression and phosphate availability in freshwater organisms, and suggest that some of the excess methane in the Lake Matano surface water, and in other methane-rich lakes, may be produced by P-starved bacteria.



Methane is an important greenhouse gas, and contributes substantially to global warming. Although freshwater environments are known to release methane into the atmosphere, estimates of the amount of methane emitted by freshwater lakes vary from 8 to 73 Tg per year. Methane emissions are difficult to predict in part because the source of the methane can vary: it is the end product of the energy-conserving pathway in methanogenic archaea, which predominantly live in anoxic sediments or waters, but have also been identified in some oxic freshwater environments. More recently, methane release from small organic molecules has been observed in oxic marine environments. Here we show that demethylation of methylphosphonate may also contribute to methane release from lakes, and that phosphate can repress this activity. Since lakes are typically phosphorus-limited, some methane release in these environments may be a byproduct of phosphorus metabolism, rather than carbon or energy metabolism. Methane emissions from lakes are currently predicted using primary production, eutrophication status, extent of anoxia, and the shape and size of the lake; to improve prediction of methane emissions, phosphorus availability and sources may also need to be included in these models.
Department of Civil and Environmental Engineering, University of Delaware, Newark Delaware USA.
Mengyin
M
Yao
Research Center for Limnology, Indonesian Institute of Sciences, Cibinong Indonesia.
Cynthia
C
Henny
Department of Civil and Environmental Engineering, University of Delaware, Newark Delaware USA jmaresca@udel.edu.
Julia A
JA
Maresca
ISME J. 2016 Feb;10(2):273-86
26090992
Geobiology. 2011 Jan;9(1):61-78
20854329
Nat Commun. 2014 Oct 30;5:5350
25355035
Nature. 2015 Sep 3;525(7567):68-72
26280334
Curr Opin Chem Biol. 2013 Aug;17(4):589-96
23830682
Sci Rep. 2015 Sep 15;5:14248
26370519
J Environ Sci (China). 2013 Jun 1;25(6):1124-30
24191601
Science. 2011 Jan 7;331(6013):50
21212349
Environ Microbiol. 2014 Sep;16(9):2682-98
24118837
J Ind Microbiol Biotechnol. 2014 Feb;41(2):345-56
24271089
Proc Natl Acad Sci U S A. 2013 Dec 17;110(51):20759-64
24297932
Appl Environ Microbiol. 1998 Oct;64(10):3754-8
9758795
Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15938-43
18838679
Nucleic Acids Res. 2015 Jan;43(Database issue):D261-9
25428365
Environ Pollut. 2009 Aug-Sep;157(8-9):2507-13
19345456
Environ Microbiol. 2010 Jan;12(1):222-38
19788654
Pest Manag Sci. 2012 Jan;68(1):16-30
21681915
Mol Ecol. 2015 Sep;24(17):4449-59
26179741
Appl Environ Microbiol. 2015 Dec 18;82(5):1423-32
26682860
FEMS Microbiol Lett. 1992 Dec 15;100(1-3):133-9
1335942
J Bacteriol. 1993 Jun;175(11):3430-42
8388873
Environ Sci Technol. 2002 Aug 1;36(15):3354-61
12188365
Microbiol Mol Biol Rev. 2014 Mar;78(1):176-97
24600043
Nature. 2006 Jan 5;439(7072):68-71
16397497
Gene. 1993 Jul 15;129(1):27-32
8335257
Nature. 2013 Jul 25;499(7459):431-7
23851394
Science. 2012 Aug 31;337(6098):1104-7
22936780
Environ Pollut. 2009 Jan;157(1):49-56
18804318
FEMS Microbiol Lett. 1999 Jan 1;170(1):265-70
9919677
Geobiology. 2015 Sep;13(5):454-61
25923883
Environ Sci Technol. 2015 Jun 16;49(12):7197-207
25992592
PeerJ. 2013 Feb 19;1:e23
23638358
Environ Microbiol. 2016 Feb;18(2):656-67
26415900
Environ Microbiol Rep. 2009 Oct;1(5):285-92
23765881
Annu Rev Microbiol. 2007;61:379-400
18035609
Front Microbiol. 2013 Nov 26;4:340
24324460
J Bacteriol. 1970 Apr;102(1):43-51
5437731
Nat Commun. 2014 Jul 07;5:4346
25000228
Geobiology. 2014 Jul;12(4):322-39
24923179
Environ Microbiol. 2006 May;8(5):939-45
16623750
Water Sci Technol. 2016 Nov;74(9):2075-2086
27842027
Glob Chang Biol. 2015 Mar;21(3):1124-39
25220765
Ecol Lett. 2007 Dec;10(12):1135-42
17922835
Environ Monit Assess. 2012 Sep;184(9):5829-39
22322407
Proc Natl Acad Sci U S A. 2011 Dec 6;108(49):19657-61
22089233
Microb Ecol. 2011 Nov;62(4):824-37
21735153
Front Microbiol. 2014 Nov 04;5:522
25408683
Biochim Biophys Acta. 1989 Aug 31;997(3):193-8
2504289
Nat Rev Microbiol. 2013 Jun;11(6):412-9
23624813
BMC Genomics. 2013 Nov 02;14:753
24180241
Curr Opin Chem Biol. 2013 Aug;17(4):580-8
23870698
FEMS Microbiol Ecol. 2014 Oct;90(1):78-91
24965962
Nature. 2011 Nov 16;480(7378):570-3
22089136
Science. 2006 Jun 2;312(5778):1355-9
16741115
Environ Microbiol. 2007 Oct;9(10):2392-400
17803765