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1.
Nature ; 591(7850): 445-450, 2021 03.
Article in English | MEDLINE | ID: mdl-33658719

ABSTRACT

Mitochondria are specialized eukaryotic organelles that have a dedicated function in oxygen respiration and energy production. They evolved about 2 billion years ago from a free-living bacterial ancestor (probably an alphaproteobacterium), in a process known as endosymbiosis1,2. Many unicellular eukaryotes have since adapted to life in anoxic habitats and their mitochondria have undergone further reductive evolution3. As a result, obligate anaerobic eukaryotes with mitochondrial remnants derive their energy mostly from fermentation4. Here we describe 'Candidatus Azoamicus ciliaticola', which is an obligate endosymbiont of an anaerobic ciliate and has a dedicated role in respiration and providing energy for its eukaryotic host. 'Candidatus A. ciliaticola' contains a highly reduced 0.29-Mb genome that encodes core genes for central information processing, the electron transport chain, a truncated tricarboxylic acid cycle, ATP generation and iron-sulfur cluster biosynthesis. The genome encodes a respiratory denitrification pathway instead of aerobic terminal oxidases, which enables its host to breathe nitrate instead of oxygen. 'Candidatus A. ciliaticola' and its ciliate host represent an example of a symbiosis that is based on the transfer of energy in the form of ATP, rather than nutrition. This discovery raises the possibility that eukaryotes with mitochondrial remnants may secondarily acquire energy-providing endosymbionts to complement or replace functions of their mitochondria.


Subject(s)
Anaerobiosis , Bacteria/metabolism , Ciliophora/metabolism , Denitrification , Energy Metabolism , Host Microbial Interactions , Symbiosis , Adenosine Triphosphate/metabolism , Bacteria/genetics , Biological Evolution , Cell Respiration , Ciliophora/chemistry , Ciliophora/cytology , Citric Acid Cycle/genetics , Electron Transport/genetics , Genome, Bacterial/genetics , Host Microbial Interactions/genetics , Mitochondria , Nitrates/metabolism , Oxygen/metabolism , Phylogeny
2.
Nature ; 600(7887): 105-109, 2021 12.
Article in English | MEDLINE | ID: mdl-34732889

ABSTRACT

Symbiotic N2-fixing microorganisms have a crucial role in the assimilation of nitrogen by eukaryotes in nitrogen-limited environments1-3. Particularly among land plants, N2-fixing symbionts occur in a variety of distantly related plant lineages and often involve an intimate association between host and symbiont2,4. Descriptions of such intimate symbioses are lacking for seagrasses, which evolved around 100 million years ago from terrestrial flowering plants that migrated back to the sea5. Here we describe an N2-fixing symbiont, 'Candidatus Celerinatantimonas neptuna', that lives inside seagrass root tissue, where it provides ammonia and amino acids to its host in exchange for sugars. As such, this symbiosis is reminiscent of terrestrial N2-fixing plant symbioses. The symbiosis between Ca. C. neptuna and its host Posidonia oceanica enables highly productive seagrass meadows to thrive in the nitrogen-limited Mediterranean Sea. Relatives of Ca. C. neptuna occur worldwide in coastal ecosystems, in which they may form similar symbioses with other seagrasses and saltmarsh plants. Just like N2-fixing microorganisms might have aided the colonization of nitrogen-poor soils by early land plants6, the ancestors of Ca. C. neptuna and its relatives probably enabled flowering plants to invade nitrogen-poor marine habitats, where they formed extremely efficient blue carbon ecosystems7.


Subject(s)
Alismatales/microbiology , Aquatic Organisms/metabolism , Bacteria/metabolism , Nitrogen Fixation , Nitrogen/metabolism , Symbiosis , Alismatales/metabolism , Amino Acids/metabolism , Ammonia/metabolism , Aquatic Organisms/microbiology , Ecosystem , Endophytes/metabolism , Mediterranean Sea , Plant Leaves/metabolism , Plant Roots/metabolism , Plant Roots/microbiology
3.
Proc Natl Acad Sci U S A ; 115(43): 10926-10931, 2018 10 23.
Article in English | MEDLINE | ID: mdl-30301807

ABSTRACT

Terrestrial paleoclimate archives such as lake sediments are essential for our understanding of the continental climate system and for the modeling of future climate scenarios. However, quantitative proxies for the determination of paleotemperatures are sparse. The relative abundances of certain bacterial lipids, i.e., branched glycerol dialkyl glycerol tetraethers (brGDGTs), respond to changes in environmental temperature, and thus have great potential for climate reconstruction. Their application to lake deposits, however, is hampered by the lack of fundamental knowledge on the ecology of brGDGT-producing microbes in lakes. Here, we show that brGDGTs are synthesized by multiple groups of bacteria thriving under contrasting redox regimes in a deep meromictic Swiss lake (Lake Lugano). This niche partitioning is evidenced by highly distinct brGDGT inventories in oxic vs. anoxic water masses, and corresponding vertical patterns in bacterial 16S rRNA gene abundances, implying that sedimentary brGDGT records are affected by temperature-independent changes in the community composition of their microbial producers. Furthermore, the stable carbon isotope composition (δ13C) of brGDGTs in Lake Lugano and 34 other (peri-)Alpine lakes attests to the widespread heterotrophic incorporation of 13C-depleted, methane-derived biomass at the redox transition zone of mesotrophic to eutrophic lake systems. The brGDGTs produced under such hypoxic/methanotrophic conditions reflect near-bottom water temperatures, and are characterized by comparatively low δ13C values. Depending on climate zone and water depth, lake sediment archives predominated by deeper water/low-13C brGDGTs may provide more reliable records of climate variability than those where brGDGTs derive from terrestrial and/or aquatic sources with distinct temperature imprints.


Subject(s)
Bacteria/metabolism , Glycerol/metabolism , Lakes/microbiology , Lipids/chemistry , Biomass , Carbon/metabolism , Carbon Isotopes/metabolism , Ecology , Geologic Sediments/microbiology , Methane/metabolism , Oxidation-Reduction , RNA, Ribosomal, 16S/metabolism
4.
Environ Microbiol ; 21(5): 1611-1626, 2019 05.
Article in English | MEDLINE | ID: mdl-30689286

ABSTRACT

Anoxygenic phototrophic sulfide oxidation by green and purple sulfur bacteria (PSB) plays a key role in sulfide removal from anoxic shallow sediments and stratified waters. Although some PSB can also oxidize sulfide with nitrate and oxygen, little is known about the prevalence of this chemolithotrophic lifestyle in the environment. In this study, we investigated the role of these phototrophs in light-independent sulfide removal in the chemocline of Lake Cadagno. Our temporally resolved, high-resolution chemical profiles indicated that dark sulfide oxidation was coupled to high oxygen consumption rates of ~9 µM O2 ·h-1 . Single-cell analyses of lake water incubated with 13 CO2 in the dark revealed that Chromatium okenii was to a large extent responsible for aerobic sulfide oxidation and it accounted for up to 40% of total dark carbon fixation. The genome of Chr. okenii reconstructed from the Lake Cadagno metagenome confirms its capacity for microaerophilic growth and provides further insights into its metabolic capabilities. Moreover, our genomic and single-cell data indicated that other PSB grow microaerobically in these apparently anoxic waters. Altogether, our observations suggest that aerobic respiration may not only play an underappreciated role in anoxic environments but also that organisms typically considered strict anaerobes may be involved.


Subject(s)
Chromatiaceae/metabolism , Lakes/microbiology , Oxygen/metabolism , Sulfides/metabolism , Aerobiosis , Chromatiaceae/genetics , Chromatiaceae/growth & development , Chromatiaceae/radiation effects , Lakes/analysis , Light , Oxidation-Reduction , Oxygen/analysis , Phototrophic Processes
5.
Environ Microbiol ; 20(7): 2598-2614, 2018 07.
Article in English | MEDLINE | ID: mdl-29806730

ABSTRACT

Methanotrophic bacteria represent an important biological filter regulating methane emissions into the atmosphere. Planktonic methanotrophic communities in freshwater lakes are typically dominated by aerobic gamma-proteobacteria, with a contribution from alpha-proteobacterial methanotrophs and the NC10 bacteria. The NC10 clade encompasses methanotrophs related to 'Candidatus Methylomirabilis oxyfera', which oxidize methane using a unique pathway of denitrification that tentatively produces N2 and O2 from nitric oxide (NO). Here, we describe a new species of the NC10 clade, 'Ca. Methylomirabilis limnetica', which dominated the planktonic microbial community in the anoxic depths of the deep stratified Lake Zug in two consecutive years, comprising up to 27% of the total bacterial population. Gene transcripts assigned to 'Ca. M. limnetica' constituted up to one third of all metatranscriptomic sequences in situ. The reconstructed genome encoded a complete pathway for methane oxidation, and an incomplete denitrification pathway, including two putative nitric oxide dismutase genes. The genome of 'Ca. M. limnetica' exhibited features possibly related to genome streamlining (i.e. less redundancy of key metabolic genes) and adaptation to its planktonic habitat (i.e. gas vesicle genes). We speculate that 'Ca. M. limnetica' temporarily bloomed in the lake during non-steady-state conditions suggesting a niche for NC10 bacteria in the lacustrine methane and nitrogen cycle.


Subject(s)
Bacteria, Anaerobic/isolation & purification , Denitrification , Lakes/microbiology , Methane/metabolism , Bacteria, Anaerobic/classification , Bacteria, Anaerobic/genetics , Bacteria, Anaerobic/metabolism , Genome, Bacterial , Microbiota , Nitric Oxide/metabolism , Nitrogen Cycle , Oxidation-Reduction , Water Microbiology
6.
Environ Microbiol ; 18(12): 5288-5302, 2016 12.
Article in English | MEDLINE | ID: mdl-27768826

ABSTRACT

Iron redox reactions play an important role in carbon remineralization, supporting large microbial communities in iron-rich terrestrial and aquatic sediments. Stratified water columns with comparably low iron concentrations are globally widespread, but microbial iron cycling in these systems has largely been ignored. We found evidence for unexpectedly high iron turnover rates in the low (1-2 µmol·l-1 ) iron waters of Lake Cadagno. Light-dependent, biological iron oxidation rates (1.4-13.8 µmol·l-1 ·d-1 ) were even higher than in ferruginous lakes with well-studied microbial iron cycles. This photoferrotrophic iron oxidation may account for up to 10% of total primary production in the chemocline. Iron oxides could not be detected and were presumably reduced immediately by iron-reducing microorganisms. Sequences of putative iron oxidizers and reducers were retrieved from in situ 16S rRNA gene amplicon libraries and some of these bacteria were identified in our enrichment cultures supplemented with Fe(II) and FeS. Based on our results, we propose a model in which iron is oxidized by photoferrotrophs and microaerophiles, and iron oxides are immediately reduced by heterotrophic iron reducers, resulting in a cryptic iron cycle. We hypothesize that microbial iron cycling may be more prevalent in water column redoxclines, especially those within the photic zone, than previously believed.


Subject(s)
Bacteria/metabolism , Iron/metabolism , Lakes/microbiology , Bacteria/genetics , Bacteria/isolation & purification , Carbon/metabolism , Iron/chemistry , Lakes/chemistry , Oxidation-Reduction , RNA, Ribosomal, 16S/genetics
7.
Proc Natl Acad Sci U S A ; 108(3): 1011-5, 2011 Jan 18.
Article in English | MEDLINE | ID: mdl-21199952

ABSTRACT

Despite the importance of the nitrogen (N) cycle on marine productivity, little is known about variability in N sources and cycling in the ocean in relation to natural and anthropogenic climate change. Beyond the last few decades of scientific observation, knowledge depends largely on proxy records derived from nitrogen stable isotopes (δ(15)N) preserved in sediments and other bioarchives. Traditional bulk δ(15)N measurements, however, represent the combined influence of N source and subsequent trophic transfers, often confounding environmental interpretation. Recently, compound-specific analysis of individual amino acids (δ(15)N-AA) has been shown as a means to deconvolve trophic level versus N source effects on the δ(15)N variability of bulk organic matter. Here, we demonstrate the first use of δ(15)N-AA in a paleoceanographic study, through analysis of annually secreted growth rings preserved in the organic endoskeletons of deep-sea gorgonian corals. In the Northwest Atlantic off Nova Scotia, coral δ(15)N is correlated with increasing presence of subtropical versus subpolar slope waters over the twentieth century. By using the new δ(15)N-AA approach to control for variable trophic processing, we are able to interpret coral bulk δ(15)N values as a proxy for nitrate source and, hence, slope water source partitioning. We conclude that the persistence of the warm, nutrient-rich regime since the early 1970s is largely unique in the context of the last approximately 1,800 yr. This evidence suggests that nutrient variability in this region is coordinated with recent changes in global climate and underscores the broad potential of δ(15)N-AA for paleoceanographic studies of the marine N cycle.


Subject(s)
Anthozoa/chemistry , Climate Change , Environmental Monitoring/statistics & numerical data , Nitrogen Isotopes/analysis , Amino Acids/analysis , Animals , Atlantic Ocean , Environmental Monitoring/methods , Mass Spectrometry , Nova Scotia , Paleontology , Temperature
8.
Sci Adv ; 10(4): eadi0617, 2024 Jan 26.
Article in English | MEDLINE | ID: mdl-38266091

ABSTRACT

The extent of littoral influence on lake gas dynamics remains debated in the aquatic science community due to the lack of direct quantification of lateral gas transport. The prevalent assumption of diffusive horizontal transport in gas budgets fails to explain anomalies observed in pelagic gas concentrations. Here, we demonstrate through high-frequency measurements in a eutrophic lake that daily convective horizontal circulation generates littoral-pelagic advective gas fluxes one order of magnitude larger than typical horizontal fluxes used in gas budgets. These lateral fluxes are sufficient to redistribute gases at the basin-scale and generate concentration anomalies reported in other lakes. Our observations also contrast the hypothesis of pure, nocturnal littoral-to-pelagic exchange by showing that convective circulation transports gases such as oxygen and methane toward both the pelagic and littoral zones during the daytime. This study challenges the traditional pelagic-centered models of aquatic systems by showing that convective circulation represents a fundamental lateral transport mechanism to be integrated into gas budgets.

9.
Nat Commun ; 15(1): 5293, 2024 Jun 21.
Article in English | MEDLINE | ID: mdl-38906896

ABSTRACT

Lacustrine methane emissions are strongly mitigated by aerobic methane-oxidizing bacteria (MOB) that are typically most active at the oxic-anoxic interface. Although oxygen is required by the MOB for the first step of methane oxidation, their occurrence in anoxic lake waters has raised the possibility that they are capable of oxidizing methane further anaerobically. Here, we investigate the activity and growth of MOB in Lake Zug, a permanently stratified freshwater lake. The rates of anaerobic methane oxidation in the anoxic hypolimnion reached up to 0.2 µM d-1. Single-cell nanoSIMS measurements, together with metagenomic and metatranscriptomic analyses, linked the measured rates to MOB of the order Methylococcales. Interestingly, their methane assimilation activity was similar under hypoxic and anoxic conditions. Our data suggest that these MOB use fermentation-based methanotrophy as well as denitrification under anoxic conditions, thus offering an explanation for their widespread presence in anoxic habitats such as stratified water columns. Thus, the methane sink capacity of anoxic basins may have been underestimated by not accounting for the anaerobic MOB activity.


Subject(s)
Lakes , Methane , Oxidation-Reduction , Methane/metabolism , Lakes/microbiology , Anaerobiosis , Methylococcaceae/metabolism , Methylococcaceae/genetics , Metagenomics , Oxygen/metabolism
10.
ISME Commun ; 4(1): ycae089, 2024 Jan.
Article in English | MEDLINE | ID: mdl-38988698

ABSTRACT

Emissions of microbially produced methane (CH4) from lake sediments are a major source of this potent greenhouse gas to the atmosphere. The rates of CH4 production and emission are believed to be influenced by electron acceptor distributions and organic carbon contents, which in turn are affected by anthropogenic inputs of nutrients leading to eutrophication. Here, we investigate how eutrophication influences the abundance and community structure of CH4 producing Archaea and methanogenesis pathways across time-resolved sedimentary records of five Swiss lakes with well-characterized trophic histories. Despite higher CH4 concentrations which suggest higher methanogenic activity in sediments of eutrophic lakes, abundances of methanogens were highest in oligotrophic lake sediments. Moreover, while the methanogenic community composition differed significantly at the lowest taxonomic levels (OTU), depending on whether sediment layers had been deposited under oligotrophic or eutrophic conditions, it showed no clear trend in relation to in situ distributions of electron acceptors. Remarkably, even though methanogenesis from CO2-reduction was the dominant pathway in all sediments based on carbon isotope fractionation values, taxonomic identities, and genomes of resident methanogens, CO2-reduction with hydrogen (H2) was thermodynamically unfavorable based on measured reactant and product concentrations. Instead, strong correlations between genomic abundances of CO2-reducing methanogens and anaerobic bacteria with potential for extracellular electron transfer suggest that methanogenic CO2-reduction in lake sediments is largely powered by direct electron transfer from syntrophic bacteria without involvement of H2 as an electron shuttle.

11.
PLoS One ; 18(11): e0281828, 2023.
Article in English | MEDLINE | ID: mdl-37939036

ABSTRACT

Lake Tanganyika's pelagic fish sustain the second largest inland fishery in Africa and are under pressure from heavy fishing and global warming related increases in stratification. The strength of water column stratification varies regionally, with a more stratified north and an upwelling-driven, biologically more productive south. Only little is known about whether such regional hydrodynamic regimes induce ecological or genetic differences among populations of highly mobile, pelagic fish inhabiting these different areas. Here, we examine whether the regional contrasts leave distinct isotopic imprints in the pelagic fish of Lake Tanganyika, which may reveal differences in diet or lipid content. We conducted two lake-wide campaigns during different seasons and collected physical, nutrient, chlorophyll, phytoplankton and zooplankton data. Additionally, we analyzed the pelagic fish-the clupeids Stolothrissa tanganicae, Limnothrissa miodon and four Lates species-for their isotopic and elemental carbon (C) and nitrogen (N) compositions. The δ13C values were significantly higher in the productive south after the upwelling/mixing period across all trophic levels, implying that the fish have regional foraging grounds, and thus record these latitudinal isotope gradients. By combining our isotope data with previous genetic results showing little geographic structure, we demonstrate that the fish reside in a region for a season or longer. Between specimens from the north and south we found no strong evidence for varying trophic levels or lipid contents, based on their bulk δ15N and C:N ratios. We suggest that the development of regional trophic or physiological differences may be inhibited by the lake-wide gene flow on the long term. Overall, our findings show that the pelagic fish species, despite not showing evidence for genetic structure at the basin scale, form regional stocks at the seasonal timescales. This implies that sustainable management strategies may consider adopting regional fishing quotas.


Subject(s)
Carbon , Lakes , Animals , Tanzania , Isotopes , Lipids , Food Chain , Fishes
12.
Nat Commun ; 14(1): 6591, 2023 10 18.
Article in English | MEDLINE | ID: mdl-37852975

ABSTRACT

The factors that govern the geographical distribution of nitrogen fixation are fundamental to providing accurate nitrogen budgets in aquatic environments. Model-based insights have demonstrated that regional hydrodynamics strongly impact nitrogen fixation. However, the mechanisms establishing this physical-biological coupling have yet to be constrained in field surveys. Here, we examine the distribution of nitrogen fixation in Lake Tanganyika - a model system with well-defined hydrodynamic regimes. We report that nitrogen fixation is five times higher under stratified than under upwelling conditions. Under stratified conditions, the limited resupply of inorganic nitrogen to surface waters, combined with greater light penetration, promotes the activity of bloom-forming photoautotrophic diazotrophs. In contrast, upwelling conditions support predominantly heterotrophic diazotrophs, which are uniquely suited to chemotactic foraging in a more dynamic nutrient landscape. We suggest that these hydrodynamic regimes (stratification versus mixing) play an important role in governing both the rates and the mode of nitrogen fixation.


Subject(s)
Lakes , Nitrogen Fixation , Hydrodynamics , Tanzania , Nitrogen
13.
Appl Environ Microbiol ; 78(3): 695-704, 2012 Feb.
Article in English | MEDLINE | ID: mdl-22101058

ABSTRACT

Chitin, which is a biopolymer of the amino sugar glucosamine (GlcN), is highly abundant in aquatic ecosystems, and its degradation is assigned a key role in the recycling of carbon and nitrogen. In order to study the significance of chitin decomposition in two temperate freshwater lakes with contrasting trophic and redox conditions, we measured the turnover rate of the chitin analog methylumbelliferyl-N,N'-diacetylchitobioside (MUF-DC) and the presence of chitinase (chiA) genes in zooplankton, water, and sediment samples. In contrast to the eutrophic and partially anoxic lake, chiA gene fragments were detectable throughout the oligotrophic water column and chiA copy numbers per ml of water were up to 15 times higher than in the eutrophic waters. For both lakes, the highest chiA abundance was found in the euphotic zone--the main habitat of zooplankton, but also the site of production of easily degradable algal chitin. The bulk of chitinase activity was measured in zooplankton samples and the sediments, where recalcitrant chitin is deposited. Both, chiA abundance and chitinase activity correlated well with organic carbon, nitrogen, and concentrations of particulate GlcN. Our findings show that chitin, although its overall contribution to the total organic carbon is small (~0.01 to 0.1%), constitutes an important microbial growth substrate in these temperate freshwater lakes, particularly where other easily degradable carbon sources are scarce.


Subject(s)
Bacteria/metabolism , Chitin/metabolism , Fresh Water/microbiology , Animals , Chitinases/genetics , Chitinases/metabolism , Geologic Sediments/microbiology , Hydrolysis , Hymecromone/analogs & derivatives , Hymecromone/metabolism , Oligosaccharides/metabolism , Zooplankton/microbiology
14.
Environ Sci Technol ; 46(8): 4515-22, 2012 Apr 17.
Article in English | MEDLINE | ID: mdl-22436104

ABSTRACT

Lakes are large sources of methane, held to be responsible for 18% of the radiative forcing, to the atmosphere. Periods of lake overturn (during fall/winter) are short and therefore difficult to capture with field campaigns but potentially one of the most important periods for methane emissions. We studied methane emissions using four different methods, including eddy covariance measurements, floating chambers, anchored funnels, and boundary model calculations. Whereas the first three methods agreed rather well, boundary model estimates were 5-30 times lower leading to a strong underestimation of methane fluxes from aquatic systems. These results show the importance of ebullition as the most important flux pathway and the need for continuous measurements with a large footprint covering also shallow parts of lakes. Although fluxes were high, on average 4 mmol m(-2) d(-1) during the overturn period, water column microbial methane oxidation removed 75% of the methane and only 25% of potential emissions were released to the atmosphere. Hence, this study illustrates second the importance of considering methane oxidation when estimating the flux of methane from lakes during overturn periods.


Subject(s)
Air Pollutants/analysis , Lakes/chemistry , Methane/analysis , Water Pollutants/analysis , Environmental Monitoring , Methane/metabolism , Methylococcaceae/metabolism , Models, Theoretical , Oxidation-Reduction , Switzerland , Water Microbiology , Water Movements , Water Pollutants/metabolism , Wind
15.
mSphere ; 7(1): e0101321, 2022 02 23.
Article in English | MEDLINE | ID: mdl-35107340

ABSTRACT

The nitrogen (N) cycle is of global importance, as N is an essential element and a limiting nutrient in terrestrial and aquatic ecosystems. Excessive anthropogenic N fertilizer usage threatens sensitive downstream aquatic ecosystems. Although freshwater lake sediments remove N through various microbially mediated processes, few studies have investigated the microbial communities involved. In an integrated biogeochemical and microbiological study on a eutrophic and oligotrophic lake, we estimated N removal rates from pore water concentration gradients in sediments. Simultaneously, the abundance of different microbial N transformation genes was investigated using metagenomics on a seasonal and spatial scale. We observed that contrasting nutrient concentrations in sediments were associated with distinct microbial community compositions and significant differences in abundances of various N transformation genes. For both characteristics, we observed a more pronounced spatial than seasonal variability within each lake. The eutrophic Lake Baldegg showed a higher denitrification potential with higher nosZ gene (N2O reductase) abundances and higher nirS:nirK (nitrite reductase) ratios, indicating a greater capacity for complete denitrification. Correspondingly, this lake had a higher N removal efficiency. The oligotrophic Lake Sarnen, in contrast, had a higher potential for nitrification. Specifically, it harbored a high abundance of Nitrospira, including some with the potential for comammox. Our results demonstrate that knowledge of the genomic N transformation potential is important for interpreting N process rates and understanding how the lacustrine sedimentary N cycle responds to variations in trophic conditions. IMPORTANCE Anthropogenic nitrogen (N) inputs can lead to eutrophication in surface waters, especially in N-limited coastal ecosystems. Lakes effectively remove reactive N by transforming it to N2 through microbial denitrification or anammox. The rates and distributions of these microbial processes are affected by factors such as the amount and quality of settling organic material and nitrate concentrations. However, the microbial communities mediating these N transformation processes in freshwater lake sediments remain largely unknown. We provide the first seasonally and spatially resolved metagenomic analysis of the N cycle in sediments of two lakes with different trophic states. We show that lakes with different trophic states select for distinct communities of N-cycling microorganisms with contrasting functional potentials for N transformation.


Subject(s)
Lakes , Microbiota , Eutrophication , Lakes/microbiology , Nitrates/analysis , Nitrogen
16.
Sci Total Environ ; 755(Pt 2): 143500, 2021 Feb 10.
Article in English | MEDLINE | ID: mdl-33223158

ABSTRACT

Coastal lakes (CL) act as limnetic-ß-oligohaline systems located on non-tidal coastlines in fresh and salt water mixing zone. Owing to considerable terrestrial nutrient input and a high autochthonous productivity CLs release greenhouse gases (GHG) to the ambient atmosphere, however, neither emission from the system was assessed nor controls on the emission were recognized so far. In this study we attempted to quantify diffusive emissions of CH4, CO2 and N2O from CLs based on data collected from seven lakes located on a south coast of the Baltic Sea in Poland. Lake water samples were collected with quarterly resolution along salinity, water depth and wind fetch gradients. From our data it emerged that the concentrations of GHGs were determined by temperature. CH4 showed dependence on salinity, lake water depth and wind fetch. N2O was controlled by dissolved O2 and NO3- and CO2 was largely related to wind fetch. It also appeared that concentrations of N2O and CO2 were influenced by terrestrial nutrient input. The mean fluxes of CH4, CO2 and N2O for the whole system were 21.7 mg·m-2·d-1, 12.7 g·m-2·d-1 and 0.74 mg·m-2·d-1, respectively which was equivalent to 7.9 g CH4·m-2·y-1, 4.6 kg CO2·m-2·y-1 and 269 mg N2O·m-2·y-1. CH4 and N2O were released throughout the year and CO2 was predominantly emitted during winter. We showed that diffusive emissions of the GHGs showed relationships to the surface area of the lakes as well as the ratio of catchment area to lake area (CA/LA). The study would benefit from further extension with higher resolution analyses of the lakes over longer timescales and quantification of ebullitive GHG emission (CH4 in particular).

17.
Nat Commun ; 12(1): 830, 2021 02 05.
Article in English | MEDLINE | ID: mdl-33547297

ABSTRACT

In marine and freshwater oxygen-deficient zones, the remineralization of sinking organic matter from the photic zone is central to driving nitrogen loss. Deep blooms of photosynthetic bacteria, which form the suboxic/anoxic chlorophyll maximum (ACM), widespread in aquatic ecosystems, may also contribute to the local input of organic matter. Yet, the influence of the ACM on nitrogen and carbon cycling remains poorly understood. Using a suite of stable isotope tracer experiments, we examined the transformation of nitrogen and carbon under an ACM (comprising of Chlorobiaceae and Synechococcales) and a non-ACM scenario in the anoxic zone of Lake Tanganyika. We find that the ACM hosts a tight coupling of photo/litho-autotrophic and heterotrophic processes. In particular, the ACM was a hotspot of organic matter remineralization that controlled an important supply of ammonium driving a nitrification-anammox coupling, and thereby played a key role in regulating nitrogen loss in the oxygen-deficient zone.


Subject(s)
Carbon Cycle/physiology , Carbon/chemistry , Chlorobi/metabolism , Nitrogen Cycle/physiology , Nitrogen/chemistry , Synechococcus/metabolism , Ammonium Compounds/chemistry , Ammonium Compounds/metabolism , Anaerobiosis/physiology , Autotrophic Processes , Carbon/metabolism , Chlorobi/chemistry , Chlorophyll/chemistry , Chlorophyll/metabolism , Democratic Republic of the Congo , Ecosystem , Isotope Labeling , Lakes/chemistry , Lakes/microbiology , Nitrification/physiology , Nitrogen/metabolism , Oxidation-Reduction , Synechococcus/chemistry , Tanzania
18.
Aquat Sci ; 83(2): 37, 2021.
Article in English | MEDLINE | ID: mdl-33785997

ABSTRACT

Freshwater lakes are essential hotspots for the removal of excessive anthropogenic nitrogen (N) loads transported from the land to coastal oceans. The biogeochemical processes responsible for N removal, the corresponding transformation rates and overall removal efficiencies differ between lakes, however, it is unclear what the main controlling factors are. Here, we investigated the factors that moderate the rates of N removal under contrasting trophic states in two lakes located in central Switzerland. In the eutrophic Lake Baldegg and the oligotrophic Lake Sarnen, we specifically examined seasonal sediment porewater chemistry, organic matter sedimentation rates, as well as 33-year of historic water column data. We find that the eutrophic Lake Baldegg, which contributed to the removal of 20 ± 6.6 gN m-2 year-1, effectively removed two-thirds of the total areal N load. In stark contrast, the more oligotrophic Lake Sarnen contributed to 3.2 ± 4.2 gN m-2 year-1, and had removed only one-third of the areal N load. The historic dataset of the eutrophic lake revealed a close linkage between annual loads of dissolved N (DN) and removal rates (NRR = 0.63 × DN load) and a significant correlation of the concentration of bottom water nitrate and removal rates. We further show that the seasonal increase in N removal rates of the eutrophic lake correlated significantly with seasonal oxygen fluxes measured across the water-sediment interface (R2 = 0.75). We suggest that increasing oxygen enhances sediment mineralization and stimulates nitrification, indirectly enhancing denitrification activity. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00027-021-00795-7.

19.
Sci Total Environ ; 782: 146738, 2021 Aug 15.
Article in English | MEDLINE | ID: mdl-33836377

ABSTRACT

Climate warming is causing rapid spatial expansion of ocean warm pools from equatorial latitudes towards the subtropics. Sedentary coral reef inhabitants in affected areas will thus be trapped in high temperature regimes, which may become the "new normal". In this study, we used clownfish Amphiprion ocellaris as model organism to study reef fish mechanisms of thermal adaptation and determine how high temperature affects multiple lipid aspects that influence physiology and thermal tolerance. We exposed juvenile fish to two different experimental conditions, implemented over 28 days: average tropical water temperatures (26 °C, control) or average warm pool temperatures (30 °C). We then performed several analyses on fish muscle and liver tissues: i) total lipid content (%), ii) lipid peroxides, iii) fatty acid profiles, iv) lipid metabolic pathways, and v) weight as body condition metric. Results showed that lipid storage capacity in A. ocellaris was not affected by elevated temperature, even in the presence of lipid peroxides in both tissues assessed. Additionally, fatty acid profiles were unresponsive to elevated temperature, and lipid metabolic networks were consequently well conserved. Consistent with these results, we did not observe changes in fish weight at elevated temperature. There were, however, differences in fatty acid profiles between tissue types and over time. Liver showed enhanced α-linolenic and linoleic acid metabolism, which is an important pathway in stress response signaling and modulation on environmental changes. Temporal oscillations in fatty acid profiles are most likely related to intrinsic factors such as growth, which leads to the mobilization of energetic reserves between different tissues throughout time according to organism needs. Based on these results, we propose that the stability of fatty acid profiles and lipid metabolic pathways may be an important thermal adaptation feature of fish exposed to warming environments.


Subject(s)
Anthozoa , Fatty Acids , Animals , Coral Reefs , Lipids , Metabolic Networks and Pathways , Oceans and Seas , Temperature
20.
Nat Commun ; 12(1): 4774, 2021 08 06.
Article in English | MEDLINE | ID: mdl-34362886

ABSTRACT

Biological N2 fixation was key to the expansion of life on early Earth. The N2-fixing microorganisms and the nitrogenase type used in the Proterozoic are unknown, although it has been proposed that the canonical molybdenum-nitrogenase was not used due to low molybdenum availability. We investigate N2 fixation in Lake Cadagno, an analogue system to the sulfidic Proterozoic continental margins, using a combination of biogeochemical, molecular and single cell techniques. In Lake Cadagno, purple sulfur bacteria (PSB) are responsible for high N2 fixation rates, to our knowledge providing the first direct evidence for PSB in situ N2 fixation. Surprisingly, no alternative nitrogenases are detectable, and N2 fixation is exclusively catalyzed by molybdenum-nitrogenase. Our results show that molybdenum-nitrogenase is functional at low molybdenum conditions in situ and that in contrast to previous beliefs, PSB may have driven N2 fixation in the Proterozoic ocean.


Subject(s)
Chromatiaceae/metabolism , Molybdenum/metabolism , Nitrogen Fixation , Nitrogen/metabolism , Biomass , Carbon Cycle , Carbon Dioxide , Cell Size , Chromatiaceae/genetics , Metagenome , Models, Theoretical , Nitrogenase/metabolism , Oceans and Seas , Single-Cell Analysis
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