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. 2023 May;17(5):693-702.
doi: 10.1038/s41396-023-01382-4. Epub 2023 Feb 20.

Water column dynamics control nitrite-dependent anaerobic methane oxidation by Candidatus "Methylomirabilis" in stratified lake basins

Guangyi Su  1   2 , Moritz F Lehmann  3 , Jana Tischer  3 , Yuki Weber  3 , Fabio Lepori  4 , Jean-Claude Walser  5 , Helge Niemann  3   6 , Jakob Zopfi  7
Affiliations

Water column dynamics control nitrite-dependent anaerobic methane oxidation by Candidatus "Methylomirabilis" in stratified lake basins

Guangyi Su et al. ISME J. 2023 May.

Abstract

We investigated microbial methane oxidation in the water column of two connected but hydrodynamically contrasting basins of Lake Lugano, Switzerland. Both basins accumulate large amounts of methane in the water column below their chemoclines, but methane oxidation efficiently prevents methane from reaching surface waters. Here we show that in the meromictic North Basin water column, a substantial fraction of methane was eliminated through anaerobic methane oxidation (AOM) coupled to nitrite reduction by Candidatus Methylomirabilis. Incubations with 14CH4 and concentrated biomass from this basin showed enhanced AOM rates with nitrate (+62%) and nitrite (+43%). In the more dynamic South Basin, however, aerobic methanotrophs prevailed, Ca. Methylomirabilis was absent in the anoxic water column, and no evidence was found for nitrite-dependent AOM. Here, the duration of seasonal stratification and anoxia seems to be too short, relative to the slow growth rate of Ca. Methylomirabilis, to allow for the establishment of anaerobic methanotrophs, in spite of favorable hydrochemical conditions. Using 16 S rRNA gene sequence data covering nearly ten years of community dynamics, we show that Ca. Methylomirabilis was a permanent element of the pelagic methane filter in the North Basin, which proliferated during periods of stable water column conditions and became the dominant methanotroph in the system. Conversely, more dynamic water column conditions led to a decline of Ca. Methylomirabilis and induced blooms of the faster-growing aerobic methanotrophs Methylobacter and Crenothrix. Our data highlight that physical (mixing) processes and ecosystem stability are key drivers controlling the community composition of aerobic and anaerobic methanotrophs.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Water column profiles in the North Basin of Lake Lugano (November 2016).
(A) oxygen (O2) and methane (CH4) concentrations, (B) nitrate (NO3–) and nitrite (NO2–) concentrations and (C) methane oxidation rates (MOR). The gray area represents the redox transition zone, starting at O2 < 5 µM, and reaching to the depth where sulfide concentrations start to rise above background levels (see also Supplementary Fig. S3). Error bars of MOR represent standard deviations (n = 3).
Fig. 2
Fig. 2. Water column profiles in the South Basin of Lake Lugano (November 2016).
(A) oxygen (O2) and methane (CH4) concentrations, (B) nitrate (NO3–) and nitrite (NO2–) concentrations, and (C) methane oxidation rates (MOR). The gray area represents the redox transition zone, starting at O2 < 5 µM, and reaching to the depth where Fe2+ rises above background concentrations (see also Supplementary Fig. S3). Error bars of MOR represent standard deviations (n = 3).
Fig. 3
Fig. 3. Effect of different electron acceptors on AOM rates in comparison to control experiments without addition of electron acceptors (n = 6).
The incubations were conducted with concentrated biomass collected in November 2016 from anoxic water layers in both North Basin (black boxplots) and South Basin (gray boxplots), and amended with 14CH4 and different oxidants (nitrate, nitrite, sulfate) or molybdate as inhibitor of sulfate reduction. In the killed controls (n = 3; not shown) no tracer conversion was observed after 32 days.
Fig. 4
Fig. 4. Depth distribution of the main methanotrophs in the water column of Lake Lugano (November 2016).
Relative abundances of Methylobacter, Crenothrix, and Ca. Methylomirabilis in the North Basin (NB: A–C) and South Basin (SB: D–F). Data are presented as relative read abundances (in %) of 16 S rRNA gene amplicons. The redox transition zone is represented by the light-gray shaded area.
Fig. 5
Fig. 5. Pearson correlation-based network analysis of water column microbial communities in 57 North Basin water column samples from 2015 to 2018.
After filtering out ASVs with mean relative abundances of <0.1%, a total of 100 ASVs were retained for network construction. Nodes of the same color within a cluster indicate that these taxa are interconnected, and the node size indicates the centrality degree.
Fig. 6
Fig. 6. Multiannual dynamics of water column chemistry and dominant methanotrophs.
A Lake Lugano North Basin water column oxygen concentrations data from 2005–2018 (August data shown). B Concentrations of potential electron acceptors for MOB introduced into water layers ≥125 m. Boxplots show median concentration values and the interquartile range. All data from a given year are shown as individual dots (n = 192 per year). Dot color indicates the approximate sampling depth. C Multiannual dynamics of Ca. Methylomirabilis, Methylobacter sp., and Crenothrix sp.in the water column of the North Basin of Lake Lugano, starting three years after the exceptional mixing events in 2005 and 2006. Data are based on relative read abundances of 16 S rRNA gene sequences. The extension of the redox transition zone is indicated by gray bars for the different sampling timepoints.
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References

    1. Bastviken D, Cole J, Pace M, Tranvik L. Methane emissions from lakes: Dependence of lake characteristics, two regional assessments, and a global estimate. Glob Biogeochem Cy. 2004;18:GB4009. doi: 10.1029/2004GB002238. - DOI
    1. He R, Wooller MJ, Pohlman JW, Quensen J, Tiedje JM, Leigh MB. Diversity of active aerobic methanotrophs along depth profiles of arctic and subarctic lake water column and sediments. ISME J. 2012;6:1937–48. doi: 10.1038/ismej.2012.34. - DOI - PMC - PubMed
    1. Blees J, Niemann H, Wenk CB, Zopfi J, Schubert CJ, Kirf MK, et al. Micro-aerobic bacterial methane oxidation in the chemocline and anoxic water column of deep south-Alpine Lake Lugano (Switzerland) Limnol Oceanogr. 2014;59:311–24. doi: 10.4319/lo.2014.59.2.0311. - DOI
    1. Blees J, Niemann H, Wenk CB, Zopfi J, Schubert CJ, Jenzer JS, et al. Bacterial methanotrophs drive the formation of a seasonal anoxic benthic nepheloid layer in an alpine lake. Limnol Oceanogr. 2014;59:1410–20. doi: 10.4319/lo.2014.59.4.1410. - DOI
    1. Milucka J, Kirf M, Lu L, Krupke A, Lam P, Littmann S, et al. Methane oxidation coupled to oxygenic photosynthesis in anoxic waters. ISME J. 2015;9:1991–2002. doi: 10.1038/ismej.2015.12. - DOI - PMC - PubMed

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