Cynthia Henny

Deep‐water anoxygenic photosythesis in a ferruginous chemocline

Ferruginous Lake Matano, Indonesia hosts one of the deepest anoxygenic photosynthetic communities on Earth. This community is dominated by low-light adapted, BChl e-synthesizing green sulfur bacteria (GSB), which comprise ~25% of the microbial community immediately below the oxic-anoxic boundary (OAB; 115-120 m in 2010). The size of this community is dependent on the mixing regime within the lake and the depth of the OAB-at ~117 m, the GSB live near their low-light limit. Slow growth and C-fixation rates suggest that the Lake Matano GSB can be supported by sulfide even though it only accumulates to scarcely detectable (low μm to nm) concentrations. A model laboratory strain (Chlorobaculum tepidum) is indeed able to access HS- for oxidation at nm concentrations. Furthermore, the GSB in Lake Matano possess a full complement of S-oxidizing genes. Together, this physiological and genetic information suggests that deep-water GSB can be supported by a S-cycle, even under ferruginous conditions. The constraints we place on the metabolic capacity and physiology of GSB have important geobiological implications. Biomarkers diagnostic of GSB would be a good proxy for anoxic conditions but could not discriminate between euxinic and ferruginous states, and though GSB biomarkers could indicate a substantial GSB community, such a community may exist with very little metabolic activity. The light requirements of GSB indicate that at light levels comparable to those in the OAB of Lake Matano or the Black Sea, GSB would have contributed little to global ocean primary production, nutrient cycling, and banded iron formation (BIF) deposition in the Precambrian. Before the proliferation of oxygenic photosynthesis, shallower OABs and lower light absorption in the oceans surface waters would have permitted greater light availability to GSB, potentially leading to a greater role for GSB in global biogeochemical cycles.

Freshwater Bacteria Release Methane as a By-Product of Phosphorus Acquisition

ABSTRACT 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, and 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. IMPORTANCE 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 live predominantly 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 by-product 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.

Geomicrobiological Features of Ferruginous Sediments from Lake Towuti, Indonesia

Lake Towuti is a tectonic basin, surrounded by ultramafic rocks. Lateritic soils form through weathering and deliver abundant iron (oxy)hydroxides but very little sulfate to the lake and its sediment. To characterize the sediment biogeochemistry, we collected cores at three sites with increasing water depth and decreasing bottom water oxygen concentrations. Microbial cell densities were highest at the shallow site—a feature we attribute to the availability of labile organic matter (OM) and the higher abundance of electron acceptors due to oxic bottom water conditions. At the two other sites, OM degradation and reduction processes below the oxycline led to partial electron acceptor depletion. Genetic information preserved in the sediment as extracellular DNA (eDNA) provided information on aerobic and anaerobic heterotrophs related to Nitrospirae, Chloroflexi, and Thermoplasmatales. These taxa apparently played a significant role in the degradation of sinking OM. However, eDNA concentrations rapidly decreased with core depth. Despite very low sulfate concentrations, sulfate-reducing bacteria were present and viable in sediments at all three sites, as confirmed by measurement of potential sulfate reduction rates. Microbial community fingerprinting supported the presence of taxa related to Deltaproteobacteria and Firmicutes with demonstrated capacity for iron and sulfate reduction. Concomitantly, sequences of Ruminococcaceae, Clostridiales, and Methanomicrobiales indicated potential for fermentative hydrogen and methane production. Such first insights into ferruginous sediments showed that microbial populations perform successive metabolisms related to sulfur, iron, and methane. In theory, iron reduction could reoxidize reduced sulfur compounds and desorb OM from iron minerals to allow remineralization to methane. Overall, we found that biogeochemical processes in the sediments can be linked to redox differences in the bottom waters of the three sites, like oxidant concentrations and the supply of labile OM. At the scale of the lacustrine record, our geomicrobiological study should provide a means to link the extant subsurface biosphere to past environments.

Preservation and Significance of Extracellular DNA in Ferruginous Sediments from Lake Towuti, Indonesia

Extracellular DNA is ubiquitous in soil and sediment and constitutes a dominant fraction of environmental DNA in aquatic systems. In theory, extracellular DNA is composed of genomic elements persisting at different degrees of preservation produced by processes occurring on land, in the water column and sediment. Extracellular DNA can be taken up as a nutrient source, excreted or degraded by microorganisms, or adsorbed onto mineral matrices, thus potentially preserving information from past environments. To test whether extracellular DNA records lacustrine conditions, we sequentially extracted extracellular and intracellular DNA from anoxic sediments of ferruginous Lake Towuti, Indonesia. We applied 16S rRNA gene Illumina sequencing on both fractions to discriminate exogenous from endogenous sources of extracellular DNA in the sediment. Environmental sequences exclusively found as extracellular DNA in the sediment originated from multiple sources. For instance, Actinobacteria, Verrucomicrobia, and Acidobacteria derived from soils in the catchment. Limited primary productivity in the water column resulted in few sequences of Cyanobacteria in the oxic photic zone, whereas stratification of the water body mainly led to secondary production by aerobic and anaerobic heterotrophs. Chloroflexi and Planctomycetes, the main degraders of sinking organic matter and planktonic sequences at the water-sediment interface, were preferentially preserved during the initial phase of burial. To trace endogenous sources of extracellular DNA, we used relative abundances of taxa in the intracellular DNA to define which microbial populations grow, decline or persist at low density with sediment depth. Cell lysis became an important additional source of extracellular DNA, gradually covering previous genetic assemblages as other microbial genera became more abundant with depth. The use of extracellular DNA as nutrient by active microorganisms led to selective removal of sequences with lowest GC contents. We conclude that extracellular DNA preserved in shallow lacustrine sediments reflects the initial environmental context, but is gradually modified and thereby shifts from its stratigraphic context. Discrimination of exogenous and endogenous sources of extracellular DNA allows simultaneously addressing in-lake and post-depositional processes. In deeper sediments, the accumulation of resting stages and sequences from cell lysis would require stringent extraction and specific primers if ancient DNA is targeted.

Metabolic potential of microbial communities from ferruginous sediments: Microbial metabolisms in ferruginous sediments

Ferruginous (Fe-rich, SO4 -poor) conditions are generally restricted to freshwater sediments on Earth today, but were likely widespread during the Archean and Proterozoic Eons. Lake Towuti, Indonesia, is a large ferruginous lake that likely hosts geochemical processes analogous to those that operated in the ferruginous Archean ocean. The metabolic potential of microbial communities and related biogeochemical cycling under such conditions remain largely unknown. We combined geochemical measurements (pore water chemistry, sulfate reduction rates) with metagenomics to link metabolic potential with geochemical processes in the upper 50 cm of sediment. Microbial diversity and quantities of genes for dissimilatory sulfate reduction (dsrAB) and methanogenesis (mcrA) decrease with increasing depth, as do rates of potential sulfate reduction. The presence of taxa affiliated with known iron- and sulfate-reducers implies potential use of ferric iron and sulfate as electron acceptors. Pore-water concentrations of acetate imply active production through fermentation. Fermentation likely provides substrates for respiration with iron and sulfate as electron donors and for methanogens that were detected throughout the core. The presence of ANME-1 16S and mcrA genes suggests potential for anaerobic methane oxidation. Overall our data suggest that microbial community metabolism in anoxic ferruginous sediments support coupled Fe, S and C biogeochemical cycling.

Water Quality and Quantity Issues of Urban Lakes in Megacity Jakarta

The lakes in urban megacity Jakarta, called as “setu or situ” by the local people, play a central role in integrated water resources management. Despite its pivotal role in maintaining the balance of urban water system, they have not received sufficient attention. Rapid urban development in a very distinct urban watershed type of lake’s surroundings has impacted on the water quantity and quality of urban lakes in megacity Jakarta. Chronic problems faced by downstream area in megacity Jakarta such as flash floods in the rainy season and water scarcity in the dry season have indicated that the lakes have not been managed and functioned well. Human and nature disturbances such as shoreline encroachment, shoreline erosion, garbage dump and inflow from untreated sewage and urban runoff have polluted the lake water and reduced its volume capacity. Nearly half of the existing lakes have reduced from 10 to > 50% of its water volume capacity due to lake area shrinkage, siltation and even excessive growth of invasive macrophytes. The lakes are mostly in disturbed to damaged environmental conditions. Lakes in urban and rural villages have less in water quantity and higher solids, organic matter, nutrients and even fecal bacteria concentrations than the lakes in planned residential, high-rise residential and industrial areas types of urban surroundings. As the lakes in the urban village and industrial area, elevated toxic metal concentrations have become public concern due to lake hygiene problems. Elevated nutrient concentrations have caused the lake eutrophication, where some lakes have suffered from excessive macrophyte coverage, algal bloom even toxic cyanobacterial bloom. The urban lakes in megacity Jakarta constantly have been degrading physically and ecologically affecting its water quantity and quality which is increasing the threat to human’s health and impact future human’s resilience in urban megacity Jakarta.