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Land-use type temporarily affects active pond community structure but not gene expression patterns
(2022)
Changes in land use and agricultural intensification threaten biodiversity and ecosystem functioning of small water bodies. We studied 67 kettle holes (KH) in an agricultural landscape in northeastern Germany using landscape-scale metatranscriptomics to understand the responses of active bacterial, archaeal and eukaryotic communities to land-use type. These KH are proxies of the millions of small standing water bodies of glacial origin spread across the northern hemisphere. Like other landscapes in Europe, the study area has been used for intensive agriculture since the 1950s. In contrast to a parallel environmental DNA study that suggests the homogenization of biodiversity across KH, conceivably resulting from long-lasting intensive agriculture, land-use type affected the structure of the active KH communities during spring crop fertilization, but not a month later. This effect was more pronounced for eukaryotes than for bacteria. In contrast, gene expression patterns did not differ between months or across land-use types, suggesting a high degree of functional redundancy across the KH communities. Variability in gene expression was best explained by active bacterial and eukaryotic community structures, suggesting that these changes in functioning are primarily driven by interactions between organisms. Our results indicate that influences of the surrounding landscape result in temporary changes in the activity of different community members. Thus, even in KH where biodiversity has been homogenized, communities continue to respond to land management. This potential needs to be considered when developing sustainable management options for restoration purposes and for successful mitigation of further biodiversity loss in agricultural landscapes.
Microbe-mediated enzymatic hydrolysis of organic matter entails the production of hydrolysate, the recovery of which may be more or less efficient. The selfish uptake mechanism, recently discovered, allows microbes to hydrolyze polysaccharides and take up large oligomers, which are then degraded in the periplasmic space. By minimizing the hydrolysate loss, selfish behaviour may be profitable for free-living cells dwelling in a patchy substrate landscape. However, selfish uptake seems to be tailored to algal-derived polysaccharides, abundant in organic particles, suggesting that particle-attached microbes may use this strategy. We tracked selfish polysaccharides uptake in surface microbial communities of the northeastern Mediterranean Sea, linking the occurrence of this processing mode with microbial lifestyle. Additionally, we set up fluorescently labelled polysaccharides incubations supplying phytodetritus to investigate a 'pioneer' scenario for particle-attached microbes. Under both conditions, selfish behaviour was almost exclusively carried out by particle-attached microbes, suggesting that this mechanism may represent an advantage in the race for particle exploitation. Our findings shed light on the selfish potential of particle-attached microbes, suggesting multifaceted foraging strategies exerted by particle colonizers.
Marine macroalgae are a key primary producer in coastal ecosystems, but are often overlooked in blue carbon inventories. Large quantities of macroalgal detritus deposit on beaches, but the fate of wrack carbon (C) is little understood. If most of the wrack carbon is respired back to CO2, there would be no net carbon sequestration. However, if most of the wrack carbon is converted to bicarbonate (alkalinity) or refractory DOC, wrack deposition would represent net carbon sequestration if at least part of the metabolic products (e.g., reduced Fe and S) are permanently removed (i.e., long-term burial) and the DOC is not remineralised. To investigate the release of macroalgal C via porewater and its potential to contribute to C sequestration (blue carbon), we monitored the degradation of Ecklonia radiata in flow-through mesocosms simulating tidal flushing on sandy beaches. Over 60 days, 81% of added E. radiata organic matter (OM) decomposed. Per 1 mol of detritus C, the degradation produced 0.48 +/- 0.34 mol C of dissolved organic carbon (DOC) (59%) and 0.25 +/- 0.07 mol C of dissolved inorganic carbon (DIC) (31%) in porewater, and a small amount of CO2 (0.3 +/- 0.0 mol C; ca. 3%) which was emitted to the atmosphere. A significant amount of carbonate alkalinity was found in porewater, equating to 33% (0.27 +/- 0.05 mol C) of the total degraded C. The degradation occurred in two phases. In the first phase (days 0-3), 27% of the OM degraded, releasing highly reactive DOC. In the second phase (days 4-60), the labile DOC was converted to DIC. The mechanisms underlying E. radiata degradation were sulphate reduction and ammonification. It is likely that the carbonate alkalinity was primarily produced through sulphate reduction. The formation of carbonate alkalinity and semi-labile or refractory DOC from beach wrack has the potential to play an overlooked role in coastal carbon cycling and contribute to marine carbon sequestration.
Methane (CH4) from aquatic ecosystems contributes to about half of total global CH4 emissions to the atmosphere. Until recently, aquatic biogenic CH4 production was exclusively attributed to methanogenic archaea living under anoxic or suboxic conditions in sediments, bottom waters, and wetlands. However, evidence for oxic CH4 production (OMP) in freshwater, brackish, and marine habitats is increasing. Possible sources were found to be driven by various planktonic organisms supporting different OMP mechanisms. Surprisingly, submerged macrophytes have been fully ignored in studies on OMP, yet they are key components of littoral zones of ponds, lakes, and coastal systems. High CH4 concentrations in these zones have been attributed to organic substrate production promoting classic methanogenesis in the absence of oxygen. Here, we review existing studies and argue that, similar to terrestrial plants and phytoplankton, macroalgae and submerged macrophytes may directly or indirectly contribute to CH4 formation in oxic waters. We propose several potential direct and indirect mechanisms: (1) direct production of CH4; (2) production of CH4 precursors and facilitation of their bacterial breakdown or chemical conversion; (3) facilitation of classic methanogenesis; and (4) facilitation of CH4 ebullition. As submerged macrophytes occur in many freshwater and marine habitats, they are important in global carbon budgets and can strongly vary in their abundance due to seasonal and boom-bust dynamics. Knowledge on their contribution to OMP is therefore essential to gain a better understanding of spatial and temporal dynamics of CH4 emissions and thus to substantially reduce current uncertainties when estimating global CH4 emissions from aquatic ecosystems.
Achromatium oxaliferum is a large sulfur bacterium easily recognized by large intracellular calcium carbonate bodies. Although these bodies often fill major parts of the cells' volume, their role and specific intracellular location are unclear. In this study, we used various microscopy and staining techniques to identify the cell compartment harboring the calcium carbonate bodies. We observed that Achromatium cells often lost their calcium carbonate bodies, either naturally or induced by treatments with diluted acids, ethanol, sodium bicarbonate and UV radiation which did not visibly affect the overall shape and motility of the cells (except for UV radiation). The water-soluble fluorescent dye fluorescein easily diffused into empty cavities remaining after calcium carbonate loss. Membranes (stained with Nile Red) formed a network stretching throughout the cell and surrounding empty or filled calcium carbonate cavities. The cytoplasm (stained with FITC and SYBR Green for nucleic acids) appeared highly condensed and showed spots of dissolved Ca2+ (stained with Fura-2). From our observations, we conclude that the calcium carbonate bodies are located in the periplasm, in extra-cytoplasmic pockets of the cytoplasmic membrane and are thus kept separate from the cell's cytoplasm. This periplasmic localization of the carbonate bodies might explain their dynamic formation and release upon environmental changes.
Studies on the diversity, distribution and ecological role of Saprolegniales (Oomycota) in freshwater ecosystems are currently receiving attention due to a greater understanding of their role in carbon cycling in various aquatic ecosystems. In this study, we characterized several Saprolegniales species isolated from Anzali lagoon, Gilan province, Iran, using morphological and molecular methods. Four species of Saprolegnia were identified, including S. anisospora and S. diclina as first reports for Iran, as well as Achlya strains, which were closely related to A. bisexualis, A. debaryana and A. intricata. Evaluation of the ligno-, cellulo- and chitinolytic activities was performed using plate assay methods. Most of the Saprolegniales isolates were obtained in autumn, and nearly 50% of the strains showed chitinolytic and cellulolytic activities. However, only a few Saprolegniales strains showed lignolytic activities. This study has important implications for better understanding the ecological niche of oomycetes, and to differentiate them from morphologically similar, but functionally different aquatic fungi in freshwater ecosystems.
Pelagic bacteria can be classified into free-living and particle-attached life modes, which either dwell in the water column or attach to suspended particles. Bacteria with a generalist life style, however, can actively shift between these two habitats. Globally increasing densities of natural and artificial particles enhance habitat heterogeneity, with potential consequences for system stability and trophic transfer through aquatic food webs. To better decipher the dynamics of microbial communities, we investigated the influence of adaptive vs. fixed habitat choice on species coexistence for a simplified bacterial community by analyzing a corresponding food web model, consisting of two specialist bacterial prey species (free and attached), a generalist bacterial prey species with the ability to shift between both habitats, and two protist predators, specialized on either water or particle compartment. For simplicity we assume a shared resource pool, considering particles only for colonization but not as a source for nutrients or carbon, that is, inert particles like microplastics or inorganic sediments. The model predicts coexistence on a cyclic attractor between fixed and flexible bacteria, if the costs for adaptive habitat choice can be balanced by adaptation speed. The presence of adaptive prey dampens predator-prey cycle amplitudes, contributing to system stabilization resulting in higher mean predator biomass compared to specialist prey only. Thus, in pelagic microbial systems, flexible habitat choice at the prey level has important implications for system stability and magnitude of energy flow through the microbial loop.
The vertical distribution of chlorophyll in stratified lakes and reservoirs frequently exhibits a maximum peak deep in the water column, referred to as the deep chlorophyll maximum (DCM). DCMs are ecologically important hot spots of primary production and nutrient cycling, and their location can determine vertical habitat gradients for primary consumers. Consequently, the drivers of DCM structure regulate many characteristics of aquatic food webs and biogeochemistry. Previous studies have identified light and thermal stratification as important drivers of summer DCM depth, but their relative importance across a broad range of lakes is not well resolved. We analyzed profiles of chlorophyll fluorescence, temperature, and light during summer stratification from 100 lakes in the Global Lake Ecological Observatory Network (GLEON) and quantified two characteristics of DCM structure: depth and thickness. While DCMs do form in oligotrophic lakes, we found that they can also form in eutrophic to dystrophic lakes. Using a random forest algorithm, we assessed the relative importance of variables associated with light attenuation vs. thermal stratification for predicting DCM structure in lakes that spanned broad gradients of morphometry and transparency. Our analyses revealed that light attenuation was a more important predictor of DCM depth than thermal stratification and that DCMs deepen with increasing lake clarity. DCM thickness was best predicted by lake size with larger lakes having thicker DCMs. Additionally, our analysis demonstrates that the relative importance of light and thermal stratification on DCM structure is not uniform across a diversity of lake types.
A fast and sensitive method for the continuous determination of methane (CH4) and its stable carbon isotopic values (delta C-13-CH4) in surface waters was developed by applying a vacuum to a gas/liquid exchange membrane and measuring the extracted gases by a portable cavity ring-down spectroscopy analyser (M-CRDS). The M-CRDS was calibrated and characterized for CH4 concentration and delta C-13-CH4 with synthetic water standards. The detection limit of the M-CRDS for the simultaneous determination of CH4 and delta C-13-CH4 is 3.6 nmol L-1 CH4. A measurement precision of CH4 concentrations and delta C-13-CH4 in the range of 1.1%, respectively, 1.7 parts per thousand (1 sigma) and accuracy (1.3%, respectively, 0.8 parts per thousand [1 sigma]) was achieved for single measurements and averaging times of 10 min. The response time tau of 57 +/- 5 s allow determination of delta C-13-CH4 values more than twice as fast than other methods. The demonstrated M-CRDS method was applied and tested for Lake Stechlin (Germany) and compared with the headspace-gas chromatography and fast membrane CH4 concentration methods. Maximum CH4 concentrations (577 nmol L-1) and lightest delta C-13-CH4 (-35.2 parts per thousand) were found around the thermocline in depth profile measurements. The M-CRDS-method was in good agreement with other methods. Temporal variations in CH4 concentration and delta C-13-CH4 obtained in 24 h measurements indicate either local methane production/oxidation or physical variations in the thermocline. Therefore, these results illustrate the need of fast and sensitive analyses to achieve a better understanding of different mechanisms and pathways of CH4 formation in aquatic environments.
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.
Bacteria play key roles in the function and diversity of aquatic systems, but aside from study of specific bloom systems, little is known about the diversity or biogeography of bacteria associated with harmful cyanobacterial blooms (cyanoHABs). CyanoHAB species are known to shape bacterial community composition and to rely on functions provided by the associated bacteria, leading to the hypothesized cyanoHAB interactome, a coevolved community of synergistic and interacting bacteria species, each necessary for the success of the others. Here, we surveyed the microbiome associated with Microcystis aeruginosa during blooms in 12 lakes spanning four continents as an initial test of the hypothesized Microcystis interactome. We predicted that microbiome composition and functional potential would be similar across blooms globally. Our results, as revealed by 16S rRNA sequence similarity, indicate that M. aeruginosa is cosmopolitan in lakes across a 280 degrees longitudinal and 90 degrees latitudinal gradient. The microbiome communities were represented by a wide range of operational taxonomic units and relative abundances. Highly abundant taxa were more related and shared across most sites and did not vary with geographic distance, thus, like Microcystis, revealing no evidence for dispersal limitation. High phylogenetic relatedness, both within and across lakes, indicates that microbiome bacteria with similar functional potential were associated with all blooms. While Microcystis and the microbiome bacteria shared many genes, whole-community metagenomic analysis revealed a suite of biochemical pathways that could be considered complementary. Our results demonstrate a high degree of similarity across global Microcystis blooms, thereby providing initial support for the hypothesized Microcystis interactome.
There is now increasing evidence for the importance of microbial regulation of biogeochemical cycling in streams. Resource availability shapes microbial community structure, but less is known about how landscape-mediated availability of nutrients and carbon can control microbial functions in streams. Using comparative metagenomics, we examined the relationship between microbial functional genes and composition of dissolved organic matter (DOM), nutrients, and suspended microbial communities in 11 streams, divided into three groups based on the predominant land cover category (agriculture, forested, or wetland). Using weighted gene co-occurrence network analysis, we identified clusters of functions related to DOM composition, agricultural land use, and/or wetland and forest land cover. Wetland-dominated streams were characterized by functions related to nitrogen metabolism and processing of aromatic carbon compounds, with strong positive correlations with dissolved organic carbon concentration and DOM aromaticity. Forested streams were characterized by metabolic functions related to monomer uptake and carbohydrates, such as mannose and fructose metabolism. In agricultural streams, microbial functions were correlated with more labile, protein-like DOM, PO4, and NO3, likely reflecting functional adaptation to labile DOM and higher nutrient concentrations. Distinct changes in the functional composition and loss of functional diversity of microorganisms became evident when comparing natural to agricultural catchments. Although all streams showed signs of functional redundancy, loss of species richness per function in agricultural catchments suggests that microbial functions in natural catchments may be more resilient to disturbance. Our results provide new insight into microbial community functions involved in nutrient and carbon biogeochemical cycles and their dependence on specific environmental settings.
Microbial communities are essential components of aquatic ecosystems through their contribution to food web dynamics and biogeochemical processes. Aquatic microbial diversity is immense and a general challenge is to understand how metabolism and interactions of single organisms shape microbial community dynamics and ecosystem-scale biogeochemical transformations. Metagenomic approaches have developed rapidly, and proven to be powerful in linking microbial community dynamics to biogeochemical processes. In this review, we provide an overview of metagenomic approaches, followed by a discussion on some recent insights they have provided, including those in this special issue. These include the discovery of new taxa and metabolisms in aquatic microbiomes, insights into community assembly and functional ecology as well as evolutionary processes shaping microbial genomes and microbiomes, and the influence of human activities on aquatic microbiomes. Given that metagenomics can now be considered a mature technology where data generation and descriptive analyses are relatively routine and informative, we then discuss metagenomic-enabled research avenues to further link microbial dynamics to biogeochemical processes. These include the integration of metagenomics into well-designed ecological experiments, the use of metagenomics to inform and validate metabolic and biogeochemical models, and the pressing need for ecologically relevant model organisms and simple microbial systems to better interpret the taxonomic and functional information integrated in metagenomes. These research avenues will contribute to a more mechanistic and predictive understanding of links between microbial dynamics and biogeochemical cycles. Owing to rapid climate change and human impacts on aquatic ecosystems, the urgency of such an understanding has never been greater.
Studies on the ecological role of fungi and, to a lesser extent, oomycetes, are receiving increasing attention, mainly due to their participation in the cycling of organic matter in aquatic ecosystems. To unravel their importance in humification processes, we isolated several strains of fungi and oomycetes from Anzali lagoon, Iran. We then performed taxonomic characterization by morphological and molecular methods, analyzed the ability to degrade several polymeric substrates, performed metabolic fingerprinting with Ecoplates, and determined the degradation of humic substances (HS) using liquid chromatography-organic carbon detection. Our analyses highlighted the capacity of aquatic fungi to better degrade a plethora of organic molecules, including complex polymers. Specifically, we were able to demonstrate not only the utilization of these complex polymers, but also the role of fungi in the production of HS. In contrast, oomycetes, despite some morphological and physiological similarities with aquatic fungi, exhibited a propensity toward opportunism, quickly benefitting from the availability of small organic molecules, while exhibiting sensitivity toward more complex polymers. Despite their contrasting roles, our study highlights the importance of both oomycetes and fungi in aquatic organic matter transformation and cycling with potential implications for the global carbon cycle.
Global change has complex eco-evolutionary consequences for organisms and ecosystems, but related concepts (e.g., novel ecosystems) do not cover their full range. Here we propose an umbrella concept of "ecological novelty" comprising (1) a site-specific and (2) an organism-centered, eco-evolutionary perspective. Under this umbrella, complementary options for studying and communicating effects of global change on organisms, ecosystems, and landscapes can be included in a toolbox. This allows researchers to address ecological novelty from different perspectives, e.g., by defining it based on (a) categorical or continuous measures, (b) reference conditions related to sites or organisms, and (c) types of human activities. We suggest striving for a descriptive, non-normative usage of the term "ecological novelty" in science. Normative evaluations and decisions about conservation policies or management are important, but require additional societal processes and engagement with multiple stakeholders.