570 Biowissenschaften; Biologie
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Institute
Shifts among Eukaryota, Bacteria, and Archaea define the vertical organization of a lake sediment
(2017)
Background: Lake sediments harbor diverse microbial communities that cycle carbon and nutrients while being constantly colonized and potentially buried by organic matter sinking from the water column. The interaction of activity and burial remained largely unexplored in aquatic sediments. We aimed to relate taxonomic composition to sediment biogeochemical parameters, test whether community turnover with depth resulted from taxonomic replacement or from richness effects, and to provide a basic model for the vertical community structure in sediments. Methods: We analyzed four replicate sediment cores taken from 30-m depth in oligo-mesotrophic Lake Stechlin in northern Germany. Each 30-cm core spanned ca. 170 years of sediment accumulation according to Cs-137 dating and was sectioned into layers 1-4 cm thick. We examined a full suite of biogeochemical parameters and used DNA metabarcoding to examine community composition of microbial Archaea, Bacteria, and Eukaryota. Results: Community beta-diversity indicated nearly complete turnover within the uppermost 30 cm. We observed a pronounced shift from Eukaryota- and Bacteria-dominated upper layers (<5 cm) to Bacteria-dominated intermediate layers (5-14 cm) and to deep layers (>14 cm) dominated by enigmatic Archaea that typically occur in deep-sea sediments. Taxonomic replacement was the prevalent mechanism in structuring the community composition and was linked to parameters indicative of microbial activity (e.g., CO2 and CH4 concentration, bacterial protein production). Richness loss played a lesser role but was linked to conservative parameters (e.g., C, N, P) indicative of past conditions. Conclusions: By including all three domains, we were able to directly link the exponential decay of eukaryotes with the active sediment microbial community. The dominance of Archaea in deeper layers confirms earlier findings from marine systems and establishes freshwater sediments as a potential low-energy environment, similar to deep sea sediments. We propose a general model of sediment structure and function based on microbial characteristics and burial processes. An upper "replacement horizon" is dominated by rapid taxonomic turnover with depth, high microbial activity, and biotic interactions. A lower "depauperate horizon" is characterized by low taxonomic richness, more stable "low-energy" conditions, and a dominance of enigmatic Archaea.
Chytrids are a diverse group of ubiquitous true zoosporic fungi. The recent molecular discovery of a large diversity of undescribed chytrids has raised awareness on their important, but so far understudied ecological role in aquatic ecosystems. In the pelagic zone, of both freshwater and marine ecosystems, many chytrid species have been morphologically described as parasites on almost all major groups of phytoplankton. However, the majority of these parasitic chytrids has rarely been isolated and lack DNA sequence data, resulting in a large proportion of "dark taxa" in databases. Here, we report on the isolation and in-depth morphological, molecular and host range characterization of a chytrid infecting the common freshwater desmid Staurastrum sp. We provide first insights on the metabolic activity of the different chytrid development stages by using the vital dye FUN (R)-1 (2-chloro-4-[2,3-dihydro-3-methyl-[benzo-1,3-thiazol-2-yl]-methylidene]-1-phenylquinolinium iodide). Cross infection experiments suggest that this chytrid is an obligate parasite and specific for the genus Staurastrum sp. Phylogenetic analysis, based on ITS1-5.8S-ITS2 and 28S rDNA sequences, placed it in the order Rhizophydiales. Based on the unique zoospore ultrastructure, combined with thallus morphology, and molecular phylogenetic placement, we describe this parasitic chytrid as a new genus and species Staurastromyces oculus, within a new family Staurastromycetaceae. (C) 2017 Elsevier GmbH. All rights reserved.
Plastic pollution is a major global concern with several million microplastic particles entering every day freshwater ecosystems via wastewater discharge. Microplastic particles stimulate biofilm formation (plastisphere) throughout the water column and have the potential to affect microbial community structure if they accumulate in pelagic waters, especially enhancing the proliferation of biohazardous bacteria. To test this scenario, we simulated the inflow of treated wastewater into a temperate lake using a continuous culture system with a gradient of concentration of microplastic particles. We followed the effect of microplastics on the microbial community structure and on the occurrence of integrase 1 (intl), a marker associated with mobile genetic elements known as a proxy for anthropogenic effects on the spread of antimicrobial resistance genes. The abundance of intl increased in the plastisphere with increasing microplastic particle concentration, but not in the water surrounding the microplastic particles. Likewise, the microbial community on microplastic was more similar to the original wastewater community with increasing microplastic concentrations. Our results show that microplastic particles indeed promote persistence of typical indicators of microbial anthropogenic pollution in natural waters, and substantiate that their removal from treated wastewater should be prioritised. (C) 2017 Elsevier Ltd. All rights reserved.
The oceans absorb about a quarter of the annually produced anthropogenic atmospheric carbon dioxide (CO2), resulting in a decrease in surface water pH, a process termed ocean acidification (OA). Surprisingly little is known about how OA affects the physiology of heterotrophic bacteria or the coupling of heterotrophic bacteria to phytoplankton when nutrients are limited. Previous experiments were, for the most part, undertaken during productive phases or following nutrient additions designed to stimulate algal blooms. Therefore, we performed an in situ large-volume mesocosm (similar to 55 m(3)) experiment in the Baltic Sea by simulating different fugacities of CO2 (fCO(2)) extending from present to future conditions. The study was conducted in July-August after the nominal spring bloom, in order to maintain low-nutrient conditions throughout the experiment. This resulted in phytoplankton communities dominated by small-sized functional groups (picophytoplankton). There was no consistent fCO(2)-induced effect on bacterial protein production (BPP), cell-specific BPP (csBPP) or biovolumes (BVs) of either free-living (FL) or particle-associated (PA) heterotrophic bacteria, when considered as individual components (univariate analyses). Permutational Multivariate Analysis of Variance (PERMANOVA) revealed a significant effect of the fCO(2) treatment on entire assemblages of dissolved and particulate nutrients, metabolic parameters and the bacteria-phytoplankton community. However, distance-based linear modelling only identified fCO(2) as a factor explaining the variability observed amongst the microbial community composition, but not for explaining variability within the metabolic parameters. This suggests that fCO(2) impacts on microbial metabolic parameters occurred indirectly through varying physicochemical parameters and microbial species composition. Cluster analyses examining the co-occurrence of different functional groups of bacteria and phytoplankton further revealed a separation of the four fCO(2)-treated mesocosms from both control mesocosms, indicating that complex trophic interactions might be altered in a future acidified ocean. Possible consequences for nutrient cycling and carbon export are still largely unknown, in particular in a nutrient-limited ocean.
Citizen science projects have a long history in ecological studies. The research usefulness of such projects is dependent on applying simple and standardized methods. Here, we conducted a citizen science project that involved more than 3500 Swedish high school students to examine the temperature difference between surface water and the overlying air (T-w-T-a) as a proxy for sensible heat flux (Q(H)). If Q(H) is directed upward, corresponding to positive T-w-T-a, it can enhance CO2 and CH4 emissions from inland waters, thereby contributing to increased greenhouse gas concentrations in the atmosphere. The students found mostly negative T-w-T-a across small ponds, lakes, streams/rivers and the sea shore (i.e. downward Q(H)), with T-w-T-a becoming increasingly negative with increasing T-a. Further examination of T-w-T-a using high-frequency temperature data from inland waters across the globe confirmed that T-w-T-a is linearly related to T-a. Using the longest available high-frequency temperature time series from Lake Erken, Sweden, we found a rapid increase in the occasions of negative T-w-T-a with increasing annual mean T-a since 1989. From these results, we can expect that ongoing and projected global warming will result in increasingly negative T-w-T-a, thereby reducing CO2 and CH4 transfer velocities from inland waters into the atmosphere.
Aerobic anoxygenic phototrophs (AAPs) have been shown to exist in numerous marine and brackish environments where they are hypothesized to play important ecological roles. Despite their potential significance, the study of freshwater AAPs is in its infancy and limited to local investigations. Here, we explore the occurrence, diversity and distribution of AAPs in lakes covering a wide latitudinal gradient: Mongolian and German lakes located in temperate regions of Eurasia, tropical Great East African lakes, and polar permanently ice-covered Antarctic lakes. Our results show a widespread distribution of AAPs in lakes with contrasting environmental conditions and confirm that this group is composed of different members of the Alpha- and Betaproteobacteria. While latitude does not seem to strongly influence AAP abundance, clear patterns of community structure and composition along geographic regions were observed as indicated by a strong macro-geographical signal in the taxonomical composition of AAPs. Overall, our results suggest that the distribution patterns of freshwater AAPs are likely driven by a combination of small-scale environmental conditions (specific of each lake and region) and large-scale geographic factors (climatic regions across a latitudinal gradient).
Diurnally-migrating Chaoborus spp. reach populations of up to 130,000 individuals m−2 in lakes up to 70 meters deep on all continents except Antarctica. Linked to eutrophication, migrating Chaoborus spp. dwell in the anoxic sediment during daytime and feed in the oxic surface layer at night. Our experiments show that by burrowing into the sediment, Chaoborus spp. utilize the high dissolved gas partial pressure of sediment methane to inflate their tracheal sacs. This mechanism provides a significant energetic advantage that allows the larvae to migrate via passive buoyancy rather than more energy-costly swimming. The Chaoborus spp. larvae, in addition to potentially releasing sediment methane bubbles twice a day by entering and leaving the sediment, also transport porewater methane within their gas vesicles into the water column, resulting in a flux of 0.01–2 mol m−2 yr−1 depending on population density and water depth. Chaoborus spp. emerging annually as flies also result in 0.1–6 mol m−2 yr−1 of carbon export from the system. Finding the tipping point in lake eutrophication enabling this methane-powered migration mechanism is crucial for ultimately reconstructing the geographical expansion of Chaoborus spp., and the corresponding shifts in the lake’s biogeochemistry, carbon cycling and food web structure.
Benthic microbial communities (BMCs) play important roles in the carbon cycle of lakes, and benthic littoral zones in particular have been previously highlighted as biogeochemical hotspots. Dissolved organic matter (DOM) presents the major carbon pool in lakes, and although the effect of DOM composition on the pelagic microbial community composition is widely accepted, little is known about its effect on BMCs, particularly aquatic fungi. Therefore, we investigated the composition of benthic littoral microbial communities in twenty highly diverse lakes in northeast Germany. DOM quality was analyzed via size exclusion chromatography (SEC), fluorescence parallel factor analyses (PRAFACs) and UV-Vis spectroscopy. We determined the BMC composition and biomass using phospholipid-derived fatty acids (PLFA) and extended the interpretation to the analysis of fungi by applying a Bayesian mixed model. We present evidence that the quality of DOM structures the BMCs, which are dominated by heterotrophic bacteria and show low fungal biomass. The fungal biomass increases when the DOM pool is processed by microorganisms of allochthonous origin, whereas the opposite is true for bacteria.
The ecological relevance of fungi in freshwater ecosystems is becoming increasingly evident, particularly in processing the extensive amounts of polymeric organic carbon such as cellulose, chitin, and humic substances (HS). We isolated several fungal strains from oligo-mesotrophic Lake Stechlin, Brandenburg, Germany, and analyzed their ability to degrade polymeric-like substrates. Using liquid chromatography-organic carbon detection, we determined the byproducts of HS transformation by the freshwater fungus Cladosporium sp. KR14. We demonstrate the ability of this fungus to degrade and simultaneously synthesize HS, and that transformation processes were intensified when iron, as indicator of the occurrence of Fenton reactions, was present in the medium. Furthermore, we showed that structural complexity of the HS produced changed with the availability of other polymeric substances in the medium. Our study highlights the contribution of freshwater Ascomycetes to the transformation of complex organic compounds. As such, it has important implications for understanding the ecological contribution of fungi to aquatic food webs and related biogeochemical cycles.
Understanding interrelations between an environment's hydrological past and its current biogeochemistry is necessary for the assessment of biogeochemical and microbial responses to changing hydrological conditions. The question how previous dry-wet events determine the contemporary microbial and biogeochemical state is addressed in this study. Therefore, sediments exposed to the atmosphere of areas with a different hydrological past within one kettle hole, i.e. (1) the predominantly inundated pond center, (2) the pond margin frequently desiccated for longer periods and (3) an intermediate zone, were incubated with the same rewetting treatment. Physicochemical and textural characteristics were related to structural microbial parameters regarding carbon and nitrogen turnover, i.e. abundance of bacteria and fungi, denitrifiers (targeted by the nirK und nirS functional genes) and nitrate ammonifiers (targeted by the nrfA functional gene). Our study reveals that, in combination with varying sediment texture, the hydrological history creates distinct microbial habitats with defined boundary conditions within the kettle hole, mainly driven by redox conditions, pH and organic matter (OM) composition. OM mineralization, as indicated by CO2-outgassing, was most efficient in exposed sediments with a less stable hydrological past. The potential for nitrogen retention via nitrate ammonification was highest in the hydrologically rather stable pond center, counteracting nitrogen loss due to denitrification. Therefore, the degree of hydrological stability is an important factor leaving a microbial and biogeochemical legacy, which determines carbon and nitrogen losses from small lentic freshwater systems in the long term run.
Chytrids are zoosporic fungi that play an important, but yet understudied, ecological role in aquatic ecosystems. Many chytrid species have been morphologically described as parasites on phytoplankton. However, the majority of them have rarely been isolated and lack DNA sequence data. In this study we isolated and cultivated three parasitic chytrids, infecting a common volvocacean host species, Yamagishiella unicocca. To identify the chytrids, we characterized morphology and life cycle, and analyzed phylogenetic relationships based on 18S and 28S rDNA genes. Host range and specificity of the chytrids was determined by cross-infection assays with host strains, characterized by rbcL and ITS markers. We were able to confirm the identity of two chytrid strains as Endocoenobium eudorinae Ingold and Dangeardia mamillata Schroder and described the third chytrid strain as Algomyces stechlinensis gen. et sp. nov. The three chytrids were assigned to novel and phylogenetically distant clades within the phylum Chytridiomycota, each exhibiting different host specificities. By integrating morphological and molecular data of both the parasitic chytrids and their respective host species, we unveiled cryptic host-parasite associations. This study highlights that a high prevalence of (pseudo)cryptic diversity requires molecular characterization of both phytoplankton host and parasitic chytrid to accurately identify and compare host range and specificity, and to study phytoplankton-chytrid interactions in general.
Under ongoing climate change and increasing anthropogenic activity, which continuously challenge ecosystem resilience, an in-depth understanding of ecological processes is urgently needed. Lakes, as providers of numerous ecosystem services, face multiple stressors that threaten their functioning. Harmful cyanobacterial blooms are a persistent problem resulting from nutrient pollution and climate-change induced stressors, like poor transparency, increased water temperature and enhanced stratification. Consistency in data collection and analysis methods is necessary to achieve fully comparable datasets and for statistical validity, avoiding issues linked to disparate data sources. The European Multi Lake Survey (EMLS) in summer 2015 was an initiative among scientists from 27 countries to collect and analyse lake physical, chemical and biological variables in a fully standardized manner. This database includes in-situ lake variables along with nutrient, pigment and cyanotoxin data of 369 lakes in Europe, which were centrally analysed in dedicated laboratories. Publishing the EMLS methods and dataset might inspire similar initiatives to study across large geographic areas that will contribute to better understanding lake responses in a changing environment.
1. Global pressures on freshwater ecosystems are high and rising. Viewed primarily as a resource for humans, current practices of water use have led to catastrophic declines in freshwater species and the degradation of freshwater ecosystems, including their genetic and functional diversity. Approximately three-quarters of the world's inland wetlands have been lost, one-third of the 28 000 freshwater species assessed for the International Union for Conservation of Nature (IUCN) Red List are threatened with extinction, and freshwater vertebrate populations are undergoing declines that are more rapid than those of terrestrial and marine species. This global loss continues unchecked, despite the importance of freshwater ecosystems as a source of clean water, food, livelihoods, recreation, and inspiration.
2. The causes of these declines include hydrological alterations, habitat degradation and loss, overexploitation, invasive species, pollution, and the multiple impacts of climate change. Although there are policy initiatives that aim to protect freshwater life, these are rarely implemented with sufficient conviction and enforcement. Policies that focus on the development and management of fresh waters as a resource for people almost universally neglect the biodiversity that they contain.
3. Here we introduce the Alliance for Freshwater Life, a global initiative, uniting specialists in research, data synthesis, conservation, education and outreach, and policymaking. This expert network aims to provide the critical mass required for the effective representation of freshwater biodiversity at policy meetings, to develop solutions balancing the needs of development and conservation, and to better convey the important role freshwater ecosystems play in human well-being. Through this united effort we hope to reverse this tide of loss and decline in freshwater biodiversity. We introduce several short- and medium-term actions as examples for making positive change, and invite individuals, organizations, authorities, and governments to join the Alliance for Freshwater Life.
Pollution by microplastics in aquatic ecosystems is accumulating at an unprecedented scale, emerging as a new surface for biofilm formation and gene exchange. In this study, we determined the permissiveness of aquatic bacteria towards a model antibiotic resistance plasmid, comparing communities that form biofilms on microplastics vs. those that are free-living. We used an exogenous and red-fluorescent E. coli donor strain to introduce the green-fluorescent broad-host-range plasmid pKJKS which encodes for trimethoprim resistance. We demonstrate an increased frequency of plasmid transfer in bacteria associated with microplastics compared to bacteria that are free-living or in natural aggregates. Moreover, comparison of communities grown on polycarbonate filters showed that increased gene exchange occurs in a broad range of phylogenetically-diverse bacteria. Our results indicate horizontal gene transfer in this habitat could distinctly affect the ecology of aquatic microbial communities on a global scale. The spread of antibiotic resistance through microplastics could also have profound consequences for the evolution of aquatic bacteria and poses a neglected hazard for human health.
Recovering genomics clusters of secondary metabolites from lakes using genome-resolved metagenomics
(2018)
Metagenomic approaches became increasingly popular in the past decades due to decreasing costs of DNA sequencing and bioinformatics development. So far, however, the recovery of long genes coding for secondary metabolites still represents a big challenge. Often, the quality of metagenome assemblies is poor, especially in environments with a high microbial diversity where sequence coverage is low and complexity of natural communities high. Recently, new and improved algorithms for binning environmental reads and contigs have been developed to overcome such limitations. Some of these algorithms use a similarity detection approach to classify the obtained reads into taxonomical units and to assemble draft genomes. This approach, however, is quite limited since it can classify exclusively sequences similar to those available (and well classified) in the databases. In this work, we used draft genomes from Lake Stechlin, north-eastern Germany, recovered by MetaBat, an efficient binning tool that integrates empirical probabilistic distances of genome abundance, and tetranucleotide frequency for accurate metagenome binning. These genomes were screened for secondary metabolism genes, such as polyketide synthases (PKS) and non-ribosomal peptide synthases (NRPS), using the Anti-SMASH and NAPDOS workflows. With this approach we were able to identify 243 secondary metabolite clusters from 121 genomes recovered from our lake samples. A total of 18 NRPS, 19 PKS, and 3 hybrid PKS/NRPS clusters were found. In addition, it was possible to predict the partial structure of several secondary metabolite clusters allowing for taxonomical classifications and phylogenetic inferences. Our approach revealed a high potential to recover and study secondary metabolites genes from any aquatic ecosystem.
The dynamics and activities of microbes colonizing organic particles (hereafter particles) greatly determine the efficiency of the aquatic carbon pump. Current understanding is that particle composition, structure and surface properties, determined mostly by the forming organisms and organic matter, dictate initial microbial colonization and the subsequent rapid succession events taking place as organic matter lability and nutrient content change with microbial degradation. We applied a transcriptomic approach to assess the role of stochastic events on initial microbial colonization of particles. Furthermore, we asked whether gene expression corroborates rapid changes in carbon-quality. Commonly used size fractionated filtration averages thousands of particles of different sizes, sources, and ages. To overcome this drawback, we used replicate samples consisting each of 3–4 particles of identical source and age and further evaluated the consequences of averaging 10–1000s of particles. Using flow-through rolling tanks we conducted long-term experiments at near in situ conditions minimizing the biasing effects of closed incubation approaches often referred to as “the bottle-effect.” In our open flow-through rolling tank system, however, active microbial communities were highly heterogeneous despite an identical particle source, suggesting random initial colonization. Contrasting previous reports using closed incubation systems, expression of carbon utilization genes didn’t change after 1 week of incubation. Consequently, we suggest that in nature, changes in particle-associated community related to carbon availability are much slower (days to weeks) due to constant supply of labile, easily degradable organic matter. Initial, random particle colonization seems to be subsequently altered by multiple organismic interactions shaping microbial community interactions and functional dynamics. Comparative analysis of thousands particles pooled togethers as well as pooled samples suggests that mechanistic studies of microbial dynamics should be done on single particles. The observed microbial heterogeneity and inter-organismic interactions may have important implications for evolution and biogeochemistry in aquatic systems.
Heterotrophic microbes with the capability to process considerable amounts of organic matter can colonize microplastic particles (MP) in aquatic ecosystems. Weather colonization of microorganisms on MP will alter ecological niche and functioning of microbial communities remains still unanswered. Therefore, we compared the functional diversity of biofilms on microplastics when incubated in three lakes in northeastern Germany differing in trophy and limnological features. For all lakes, we compared heterotrophic activities of MP biofilms with those of microorganisms in the surrounding water by using Biolog (R) EcoPlates and assessed their oxygen consumption in microcosm assays with and without MP. The present study found that the total biofilm biomass was higher in the oligo-mesotrophic and dystrophic lakes than in the eutrophic lake. In all lakes, functional diversity profiles of MP biofilms consistently differed from those in the surrounding water. However, solely in the oligo-mesotrophic lake MP biofilms had a higher functional richness compared to the ambient water. These results demonstrate that the functionality and hence the ecological role of MP-associated microbial communities are context-dependent, i.e. different environments lead to substantial changes in biomass build up and heterotrophic activities of MP biofilms. We propose that MP surfaces act as new niches for aquatic microorganisms and that the constantly increasing MP pollution has the potential to globally impact carbon dynamics of pelagic environments by altering heterotrophic activities. (C) 2018 Elsevier B.V. All rights reserved.
Cyanobacterial mass developments impact the community composition of heterotrophic microorganisms with far-reaching consequences for biogeochemical and energy cycles of freshwater ecosystems including reservoirs. Here we sought to evaluate the temporal stability of methanogenic archaea in the water column and further scrutinize their associations with cyanobacteria. Monthly samples were collected from October 2009 to December 2010 in hypereutrophic Pampulha reservoir with permanently blooming cyanobacteria, and from January to December 2011 in oligotrophic Volta Grande reservoir with only sporadic cyanobacteria incidence. The presence of archaea in cyanobacterial cultures was investigated by screening numerous strains of Microcystis spp. from these reservoirs as well as from lakes in Europe, Asia, and North-America. We consistently determined the occurrence of archaea, in particular methanogenic archaea, in both reservoirs throughout the year. However, archaea were only associated with two strains (Microcystis sp. UFMG 165 and UFMG 175) recently isolated from these reservoirs. These findings do not implicate archaea in the occurrence of methane in the epilimnion of inland waters, but rather serve to highlight the potential of microhabitats associated with particles, including phytoplankton, to shelter unique microbial communities.