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The prevailing paradigm in aquatic science is that microbial methanogenesis happens primarily in anoxic environments. Here, we used multiple complementary approaches to show that microbial methane production could and did occur in the well-oxygenated water column of an oligotrophic lake (Lake Stechlin, Germany). Oversaturation of methane was repeatedly recorded in the well-oxygenated upper 10 m of the water column, and the methane maxima coincided with oxygen oversaturation at 6 m. Laboratory incubations of unamended epilimnetic lake water and inoculations of photoautotrophs with a lake-enrichment culture both led to methane production even in the presence of oxygen, and the production was not affected by the addition of inorganic phosphate or methylated compounds. Methane production was also detected by in-lake incubations of lake water, and the highest production rate was 1.8-2.4 nM.h(-1) at 6 m, which could explain 33-44% of the observed ambient methane accumulation in the same month. Temporal and spatial uncoupling between methanogenesis and methanotrophy was supported by field and laboratory measurements, which also helped explain the oversaturation of methane in the upper water column. Potentially methanogenic Archaea were detected in situ in the oxygenated, methane-rich epilimnion, and their attachment to photoautotrophs might allow for anaerobic growth and direct transfer of substrates for methane production. Specific PCR on mRNA of the methyl coenzyme M reductase A gene revealed active methanogenesis. Microbial methane production in oxygenated water represents a hitherto overlooked source of methane and can be important for carbon cycling in the aquatic environments and water to air methane flux.
Seasonal changes in environmental conditions have a strong impact on microbial community structure and dynamics in aquatic habitats. To better elucidate the response of bacterial communities to environmental changes, we have measured a large variety of limnetic variables and investigated bacterial community composition (BCC) and dynamics over seven consecutive years between 2003 and 2009 in mesotrophic Lake Tiefwaren (NE Germany). We separated between free-living (FL, > 0.2, < 5.0 mu m) and particle-associated (PA, > 5.0 mu m) bacteria to account for different bacterial lifestyles and to obtain a higher resolution of the microbial diversity. Changes in BCC were studied by DGGE based on PCR-amplified 16S rRNA gene fragments. Sequencing of DGGE bands revealed that ca. 70 % of all FL bacteria belonged to the Actinobacteria, whereas PA bacteria were dominated by Cyanobacteria (43 %). FL communities were generally less diverse and rather stable over time compared to their PA counterpart. Annual changes in reoccurring seasonal patterns of dominant freshwater bacteria were supported by statistical analyses, which revealed several significant correlations between DGGE profiles and various environmental variables, e.g. temperature and nutrients. Overall, FL bacteria were generally less affected by environmental changes than members of the PA fraction. Close association of PA bacteria with phytoplankton and zooplankton suggests a tight coupling of PA bacteria to organisms of higher trophic levels. Our results indicate substantial differences in bacterial lifestyle of pelagic freshwater bacteria, which are reflected by contrasting seasonal dynamics and relationships to a number of environmental variables.
Alga-bacterium interactions are crucial for aggregate formation and carbon cycling in aquatic systems. To understand the initiation of these interactions, we investigated bacterial chemotaxis within a bilateral model system. Marinobacter adhaerens HP15 has been demonstrated to attach to the diatom Thalassiosira weissflogii and induce transparent exopolymeric particle and aggregate formation. M. adhaerens possesses one polar flagellum and is highly motile. Bacterial cells were attracted to diatom cells, as demonstrated by addition of diatom cell homogenate or diatom culture supernatant to soft agar, suggesting that chemotaxis might be important for the interaction of M. adhaerens with diatoms. Three distinct chemotaxis-associated gene clusters were identified in the genome sequence of M. adhaerens, with the clusters showing significant sequence similarities to those of Pseudomonas aeruginosa PAO1. Mutations in the genes cheA, cheB, chpA, and chpB, which encode histidine kinases and methylesterases and which are putatively involved in either flagellum-associated chemotaxis or pilus-mediated twitching motility, were generated and mutants with the mutations were phenotypically analyzed. Delta cheA and Delta cheB mutants were found to be swimming deficient, and all four mutants were impaired in biofilm formation on abiotic surfaces. Comparison of the HP15 wild type and its chemotaxis mutants in cocultures with the diatom revealed that the fraction of bacteria attaching to the diatom decreased significantly for mutants in comparison to that for the wild type. Our results highlight the importance of M. adhaerens chemotaxis in initiation of its interaction with the diatom. In-depth knowledge of these basic processes in interspecies interactions is pivotal to obtain a systematic understanding of organic matter flux and nutrient cycling in marine ecosystems.
Phytoplankton development affects the community structure and dynamics of freshwater bacteria by changing the availability of nutrients, algal exudates and biological surfaces. To elucidate these effects of phytoplankton development in spring in oligotrophic Lake Stechlin (Germany), we measured limnological and biological parameters, including the bacterial community composition (BCC), at the depth of the highest chlorophyll a concentration. To increase the resolution of BCC measurements, we separated particle-associated (PA) and free-living (FL) bacteria using serial filtration through 5.0 and 0.2 mu m pore size filters, respectively. The BCC of ultramicrobacteria was also determined by collecting the 0.2 mu m filtrate on 0.1 mu m filters. Changes in the community composition of Bacteria and particularly of Actinobacteria, one of the most important bacterial groups in temperate freshwater habitats, were studied via DGGE analysis of PCR-amplified 16S rRNA gene fragments. Patterns in BCC dynamics of FL Bacteria and Actinobacteria remained fairly constant throughout the study period, while patterns of PA Bacteria were more variable over time. At the breakdown of the diatom spring bloom, bacterial production and abundance sharply increased, indicating a close coupling between heterotrophic bacteria and algal detritus. The succession in BCC revealed life-style dependent patterns related to specific environmental variables. Our results indicate independent dynamics of PA and FL Bacteria as well as Actinobacteria during succession of phytoplankton spring blooms. These differences in bacterial lifestyle can only be resolved when the PA and FL fractions of microorganisms are separated.
Environmental actinorhodopsin expression revealed by a new in situ filtration and fixation sampler
(2012)
Freshwater Actinobacteria are an important and dominant group of bacterioplankton in most temperate freshwater systems. Recently, metagenomic studies discovered rhodopsin-like protein-coding sequences present in Actinobacteria which could be a decisive hint for their success in freshwater ecosystems. We analysed the diversity of actinorhodopsin (ActR) in Lake Stechlin (northern Germany) and assessed the actR expression profile during a diurnal cycle. We obtained 85 positive actR clones which could be subsequently grouped to 17 operational taxonomic units assuming a 90% sequence similarity. The phylogenetic analysis points to a close relationship of all obtained sequences to the acI lineage of Actinobacteria, forming six independent clusters. For the first time, we followed in situ transcription of actR in Lake Stechlin revealing a rather constitutive circadian gene expression. For analysing in situ expression patterns of functional genes in aquatic ecosystems, such as actR, we invented a new in situ filtration and fixation sampler (IFFS). The IFFS enables the representative investigation of microbial transcriptomes in any aquatic ecosystem at all water depths. The IFFS sampler is simple and inexpensive, and we provide all engineering plans for an easy rebuild. Consequently, our IFFS is suitable to reliably study expression of any known functional gene of any aquatic microorganism.
Associated heterotrophic bacteria alter the microenvironment of cyanobacteria and potentially influence cyanobacterial development. Therefore, we studied interactions of the unicellular freshwater cyanobacterium Microcystis aeruginosa with heterotrophic bacteria. The associated bacterial community was greatly driven by temperature as seen by DNA fingerprinting. However, the associated microbes also closely interacted with the cyanobacteria indicating changing ecological consequence of the associated bacterial community with temperature. Whereas concentration of dissolved organic carbon in cyanobacterial cultures changed in a temperature-dependent manner, its quality greatly varied under the same environmental conditions, but with different associated bacterial communities. Furthermore, temperature affected quantity and quality of cell-bound microcystins, whereby interactions between M. aeruginosa and their associated community often masked this temperature effect. Both macro- and microenvironment of active cyanobacterial strains were characterized by high pH and oxygen values creating a unique habitat that potentially affects microbial diversity and function. For example, archaea including 'anaerobic' methanogens contributed to the associated microbial community. This implies so far uncharacterized interactions between Microcystis aeruginosa and its associated prokaryotic community, which has unknown ecological consequences in a climatically changing world.
Ciliate epibionts associated with crustacean zooplankton are widespread in aquatic systems, but their ecological roles are little known. We studied the occurrence of ciliate epibionts on crustacean zooplankton in nine German lakes with different limnological features during the summer of 2011. We also measured the detachment and re-attachment rates of the ciliates, changes in their motility, and the feeding rates of attached vs. detached ciliate epibionts. Epibionts were found in all lakes sampled except an acidic lake with large humic inputs. Epibiont prevalence was as high as 80.96% on the cladoceran Daphnia cucullata, 67.17% on the cladoceran Diaphanosoma brachyurum, and 46.67% on the calanoid copepod Eudiaptomus gracilis. Both cladoceran groups typically had less than 10 epibionts per individual, while the epibiont load on E. gracilis ranged from 1 to >30 epibionts per individual. After the death of the zooplankton host, the peritrich ciliate epibiont Epistylis sp. detached in an exponential fashion with a half-life of 5 min, and 98% detached within 30 min, leaving behind the stalks used for attachment. Immediately after detachment, the ciliates were immotile, but 62% became motile within 60 min. When a new host was present, only 27% reattached after 120 min. The average measured ingestion rate and clearance rate of Epistylis were 11,745 bacteria ciliate(-1) h(-1) and 24.33 mu l ciliate(-1) h(-1), respectively. Despite their high feeding rates, relatively low epibiont abundances were observed in the field, which suggests either diversion of energy to stalk formation, high metabolic loss by the epibionts, or high mortality among the epibiont populations.
Using the carcass sinking rate and density determined in laboratory for several freshwater zooplankton species, we developed a model of zooplankton carcass sinking as affected by turbulence and stratification. The model was subsequently used to estimate the residence time of zooplankton carcasses in the water column of Lake Stechlin, a typical temperate dimictic lake in northeastern Germany. The residence time varied among the different species and was strongly affected by thermal stratification. At the peak of summer stratification, the carcasses stayed up to 5 d in the 70 m-deep water column before reaching the lake bottom. Residence time was long enough that zooplankton carcasses could serve as an important matter and energy source for bacteria in the lake's pelagic zone and hence have the potential to significantly affect aquatic carbon and nutrient cycling. The proposed model of sinking rates, based on physically sound relationships, can be easily applied to other passively sinking particles, and be integrated into large ecosystem models.
Internal waves (seiches) are well-studied physical processes in stratified lakes, but their effects on sediment porewater chemistry and microbiology are still largely unexplored. Due to pycnocline oscillations, sediments are exposed to recurrent changes between epilimnetic and hypolimnetic water. This results in strong differences of environmental conditions, which should be reflected in the responses of redox-sensitive biogeochemical processes at both, the sediment-water interface and deeper sediment layers. We tested in a series of mesocosm experiments the influence of seiche-induced redox changes on porewater chemistry and bacterial activity in the sediments under well controlled conditions. Thereby, we excluded effects of changes in current and temperature regimes. For a period of 10 days, intact sediment cores from oligotrophic Lake Stechlin were incubated under constant (either oxic or anoxic) or alternating redox conditions. Solute concentrations were measured as porewater profiles in the sediment, while microbial activity was determined in the upper 0.5 cm of sediment. Oxic and alternating redox conditions resulted in similar ammonium, phosphate, and methane porewater concentrations, while concentrations of each analyte were considerably higher in anoxic cores. Microbial activity was clearly lower in the anoxic cores than in the oxic and the alternating cores. In conclusion, cores with intermittent anoxic phases of up to 24 hours do not differ in biogeochemistry and microbial activities from static oxic sediments. However, due to various physical processes seiches cause oxygen to penetrate deeper into sediment layers, which affects sediment redox gradients and increase microbial activity in seiche-influenced sediments.
We studied bacterial associations with the green alga Desmodesmus armatus and the diatom Stephanodiscus minutulus under changing environmental conditions and bacterial source communities, to evaluate whether bacteriaalgae associations are species-specific or more generalized and determined by external factors. Axenic and xenic algae were incubated in situ with and without allelopathically active macrophytes, and in the laboratory with sterile and nonsterile lake water and an allelochemical, tannic acid (TA). Bacterial community composition (BCC) of algae-associated bacteria was analyzed by denaturing gradient gel electrophoresis (DGGE), nonmetric multidimensional scaling, cluster analyses, and sequencing of DGGE bands. BCC of xenic algal cultures of both species were not significantly affected by changes in their environment or bacterial source community, except in the case of TA additions. Species-specific interactions therefore appear to overrule the effects of environmental conditions and source communities. The BCC of xenic and axenic D.armatus cultures subjected to in situ bacterial colonization, however, had lower similarities (ca.55%), indicating that bacterial precolonization is a strong factor for bacteriaalgae associations irrespective of environmental conditions and source community. Our findings emphasize the ecological importance of species-specific bacteriaalgae associations with important repercussions for other processes, such as the remineralization of nutrients, and organic matter dynamics.