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1.
Geobiology ; 17(3): 294-307, 2019 May.
Article in English | MEDLINE | ID: mdl-30593722

ABSTRACT

This study evaluates rates and pathways of methane (CH4 ) oxidation and uptake using 14 C-based tracer experiments throughout the oxic and anoxic waters of ferruginous Lake Matano. Methane oxidation rates in Lake Matano are moderate (0.36 nmol L-1  day-1 to 117 µmol L-1  day-1 ) compared to other lakes, but are sufficiently high to preclude strong CH4 fluxes to the atmosphere. In addition to aerobic CH4 oxidation, which takes place in Lake Matano's oxic mixolimnion, we also detected CH4 oxidation in Lake Matano's anoxic ferruginous waters. Here, CH4 oxidation proceeds in the apparent absence of oxygen (O2 ) and instead appears to be coupled to some as yet uncertain combination of nitrate ( NO 3 - ), nitrite ( NO 2 - ), iron (Fe) or manganese (Mn), or sulfate ( SO 4 2 - ) reduction. Throughout the lake, the fraction of CH4 carbon that is assimilated vs. oxidized to carbon dioxide (CO2 ) is high (up to 93%), indicating extensive CH4 conversion to biomass and underscoring the importance of CH4 as a carbon and energy source in Lake Matano and potentially other ferruginous or low productivity environments.


Subject(s)
Lakes/chemistry , Methane/chemistry , Indonesia , Oxidation-Reduction
2.
ISME J ; 12(9): 2322-2329, 2018 09.
Article in English | MEDLINE | ID: mdl-29884830

ABSTRACT

Here we present ecophysiological studies of the anaerobic sulfide oxidizers considered critical to cryptic sulfur cycling in oceanic oxygen minimum zones (OMZs). We find that HS- oxidation rates by microorganisms in the Chilean OMZ offshore from Dichato are sufficiently rapid (18 nM h-1), even at HS- concentrations well below 100 nM, to oxidize all sulfide produced during sulfate reduction in OMZs. Even at 100 nM, HS- is well below published half-saturation concentrations and we conclude that the sulfide-oxidizing bacteria in OMZs (likely the SUP05/ARTIC96BD lineage of the gammaproteobacteria) have high-affinity (>105 g-1 wet cells h-1) sulfur uptake systems. These specific affinities for sulfide are higher than those recorded for any other organism on any other substrate. Such high affinities likely allow anaerobic sulfide oxidizers to maintain vanishingly low sulfide concentrations in OMZs driving marine cryptic sulfur cycling. If more broadly distributed, such high-affinity sulfur biochemistry could facilitate sulfide-based metabolisms and prominent S-cycles in many other ostensibly sulfide-free environments.


Subject(s)
Gammaproteobacteria/metabolism , Sulfides/metabolism , Oceans and Seas , Oxidation-Reduction , Oxygen , Sulfur/metabolism
3.
Environ Microbiol ; 18(2): 656-67, 2016 Feb.
Article in English | MEDLINE | ID: mdl-26415900

ABSTRACT

Heterotrophic Proteobacteria and Actinobacteria were isolated from Lake Matano, Indonesia, a stratified, ferruginous (iron-rich), ultra-oligotrophic lake with phosphate concentrations below 50 nM. Here, we describe the growth of eight strains of heterotrophic bacteria on a variety of soluble and insoluble sources of phosphorus. When transferred to medium without added phosphorus (P), the isolates grow slowly, their RNA content falls to as low as 1% of cellular dry weight, and 86-100% of the membrane lipids are replaced with amino- or glycolipids. Similar changes in lipid composition have been observed in marine photoautotrophs and soil heterotrophs, and similar flexibility in phosphorus sources has been demonstrated in marine and soil-dwelling heterotrophs. Our results demonstrate that heterotrophs isolated from this unusual environment alter their macromolecular composition, which allows the organisms to grow efficiently even in their extremely phosphorus-limited environment.


Subject(s)
Actinobacteria/metabolism , Heterotrophic Processes/physiology , Phosphates/metabolism , Phosphorus/metabolism , Proteobacteria/metabolism , Actinobacteria/isolation & purification , Glycolipids/metabolism , Lakes/microbiology , Membrane Lipids/metabolism , Proteobacteria/isolation & purification , Water/analysis
4.
Science ; 346(6210): 735-9, 2014 Nov 07.
Article in English | MEDLINE | ID: mdl-25378621

ABSTRACT

In the low-oxygen Archean world (>2400 million years ago), seawater sulfate concentrations were much lower than today, yet open questions frustrate the translation of modern measurements of sulfur isotope fractionations into estimates of Archean seawater sulfate concentrations. In the water column of Lake Matano, Indonesia, a low-sulfate analog for the Archean ocean, we find large (>20 per mil) sulfur isotope fractionations between sulfate and sulfide, but the underlying sediment sulfides preserve a muted range of δ(34)S values. Using models informed by sulfur cycling in Lake Matano, we infer Archean seawater sulfate concentrations of less than 2.5 micromolar. At these low concentrations, marine sulfate residence times were likely 10(3) to 10(4) years, and sulfate scarcity would have shaped early global biogeochemical cycles, possibly restricting biological productivity in Archean oceans.


Subject(s)
Biological Products/history , Seawater/chemistry , Sulfates/history , Biological Products/chemical synthesis , Biological Products/chemistry , History, Ancient , Indonesia , Sulfates/analysis , Sulfur Isotopes/analysis , Sulfur Isotopes/history
5.
Proc Natl Acad Sci U S A ; 111(11): 4168-72, 2014 Mar 18.
Article in English | MEDLINE | ID: mdl-24550467

ABSTRACT

A rise in the oxygen content of the atmosphere and oceans is one of the most popular explanations for the relatively late and abrupt appearance of animal life on Earth. In this scenario, Earth's surface environment failed to meet the high oxygen requirements of animals up until the middle to late Neoproterozoic Era (850-542 million years ago), when oxygen concentrations sufficiently rose to permit the existence of animal life for the first time. Although multiple lines of geochemical evidence support an oxygenation of the Ediacaran oceans (635-542 million years ago), roughly corresponding with the first appearance of metazoans in the fossil record, the oxygen requirements of basal animals remain unclear. Here we show that modern demosponges, serving as analogs for early animals, can survive under low-oxygen conditions of 0.5-4.0% present atmospheric levels. Because the last common ancestor of metazoans likely exhibited a physiology and morphology similar to that of a modern sponge, its oxygen demands may have been met well before the enhanced oxygenation of the Ediacaran Period. Therefore, the origin of animals may not have been triggered by a contemporaneous rise in the oxygen content of the atmosphere and oceans. Instead, other ecological and developmental processes are needed to adequately explain the origin and earliest evolution of animal life on Earth.


Subject(s)
Adaptation, Biological/physiology , Atmosphere/chemistry , Biological Evolution , Microbiota/genetics , Oxygen Consumption/physiology , Oxygen/analysis , Porifera/physiology , Animals , Base Sequence , Denmark , Kinetics , Molecular Sequence Data , Polymorphism, Restriction Fragment Length , Porifera/microbiology , RNA, Ribosomal, 16S/genetics , Sequence Analysis, DNA
7.
Proc Natl Acad Sci U S A ; 105(41): 15938-43, 2008 Oct 14.
Article in English | MEDLINE | ID: mdl-18838679

ABSTRACT

Considerable discussion surrounds the potential role of anoxygenic phototrophic Fe(II)-oxidizing bacteria in both the genesis of Banded Iron Formations (BIFs) and early marine productivity. However, anoxygenic phototrophs have yet to be identified in modern environments with comparable chemistry and physical structure to the ancient Fe(II)-rich (ferruginous) oceans from which BIFs deposited. Lake Matano, Indonesia, the eighth deepest lake in the world, is such an environment. Here, sulfate is scarce (<20 micromol x liter(-1)), and it is completely removed by sulfate reduction within the deep, Fe(II)-rich chemocline. The sulfide produced is efficiently scavenged by the formation and precipitation of FeS, thereby maintaining very low sulfide concentrations within the chemocline and the deep ferruginous bottom waters. Low productivity in the surface water allows sunlight to penetrate to the >100-m-deep chemocline. Within this sulfide-poor, Fe(II)-rich, illuminated chemocline, we find a populous assemblage of anoxygenic phototrophic green sulfur bacteria (GSB). These GSB represent a large component of the Lake Matano phototrophic community, and bacteriochlorophyll e, a pigment produced by low-light-adapted GSB, is nearly as abundant as chlorophyll a in the lake's euphotic surface waters. The dearth of sulfide in the chemocline requires that the GSB are sustained by phototrophic oxidation of Fe(II), which is in abundant supply. By analogy, we propose that similar microbial communities, including populations of sulfate reducers and photoferrotrophic GSB, likely populated the chemoclines of ancient ferruginous oceans, driving the genesis of BIFs and fueling early marine productivity.


Subject(s)
Chlorobi/metabolism , Environment , Water Microbiology , Anaerobiosis , Archaea , Indonesia , Iron/metabolism , Light , Marine Biology , Molecular Sequence Data , Oxidation-Reduction , Sulfides , Sunlight
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