Identification of compounds from terrestrial dissolved organic matter toxic to cyanobacteria

Authors

Amanda D. Neilen, Anthony R. Carroll, Darryl W. Hawker, Katherine R. O’Brien, Michele A. Burford

There is emerging evidence for the phytotoxicity of terrestrial dissolved organic matter (DOM), however its sources, transformations and ecological effects in aquatic ecosystems are poorly understood. DOM characterization by Nuclear Magnetic Resonance (NMR) spectroscopy has typically involved solid-state techniques, but poor resolution has often precluded identification of individual components. This study is the first to directly identify individual phytotoxic components using a novel combined approach of preparative HPLC fractionation of DOM (obtained from leaves of two common riparian trees, Casuarina cunninghamiana and Eucalyptus tereticornis). This was followed by chemical characterization of fractions, using one-dimensional (1D) and two-dimensional (2D) solution-state ¹H NMR analyses. Additionally, the phytotoxic effect of the fractions was determined using cultures of the cyanobacteria Raphidiopsis (Cylindrospermopsis) raciborskii. The amino acid, proline, from Casuarina leachate was identified as phytotoxic, while for Eucalyptus leachate, it was gallic acid and polyphenols. These phytotoxicants remained in the leachates when they were incubated in sunlight or the dark conditions over 5 days. Our study identifies phytotoxic compounds with the potential to affect algal species composition, and potentially control nuisance R. raciborskii blooms.

Underestimated methane production triggered by phytoplankton succession in river-reservoir systems: Evidence from a microcosm study

Authors

Haolian Xu, Hong Li, Zhenzhen Tang, Yi Liu Guo Li, Qiang He

The impoundment of dammed rivers accelerates phytoplankton succession from river-dominated to lake-dominated species. Little is known about the role of phytoplankton succession in methane (CH₄) production. In this study, we performed a 61-day microcosm investigation to simulate the collapse processes of Cyclotella meneghiniana (river-dominated algae) and Chlorella pyrenoidosa and Microcystis aeruginosa (lake-dominated algae). The results suggested that different methanogenic conditions were induced by the collapse of river-and lake-dominated algae. The rapid settlement of C. meneghiniana induced aerobic conditions in the water that inhibited anaerobic CH₄ production and intensified CH₄ oxidation as a result of an increase in pmoA. However, the decomposition of C. pyrenoidosa and M. aeruginosa depleted dissolved oxygen and provided abundant labile organic matter, which jointly elevated mcrA and the mcrA/pmoA ratio. Under this condition, anaerobic CH₄ production was the dominant pathway for the mineralization of algae-derived carbon. Finally, the CH₄ produced per unit of particulate total carbon (identified as the carbon content of the algal biomass) by C. pyrenoidosa and M. aeruginosa was 16.29-fold and 8.56-fold higher, respectively, than that produced by C. meneghiniana. These observations provided evidence that lake-dominated algae played a more vital role in CH₄ production than river-dominated algae when algal succession occurred. This discovery might be a new and vital, yet largely underestimated CH₄ emission pathway in river-reservoir systems, that should be considered when evaluating the effect of hydraulic projects on greenhouse gas emissions.

Eutrophication Drives Extreme Seasonal CO2 Flux in Lake Ecosystems

Authors

Ana M. Morales-Williams, Alan D. Wanamaker Jr., Clayton J. Williams & John A. Downing

Lakes process a disproportionately large fraction of carbon relative to their size and spatial extent, representing an important component of the global carbon cycle. Alterations of ecosystem function via eutrophication change the balance of greenhouse gas flux in these systems. Without eutrophication, lakes are net sources of CO₂ to the atmosphere, but in eutrophic lakes this function may be amplified or reversed due to cycling of abundant autochthonous carbon. Using a combination of high-frequency and discrete sensor measurements, we calculated continuous CO₂ flux during the ice-free season in 15 eutrophic lakes. We found net CO₂ influx over our sampling period in 5 lakes (− 47 to − 1865 mmol m⁻²) and net efflux in 10 lakes (328 to 11,755 mmol m⁻²). Across sites, predictive models indicated that the highest efflux rates were driven by nitrogen enrichment, and influx was best predicted by chlorophyll a concentration. Regardless of whether CO₂ flux was positive or negative, stable isotope analyses indicated that the dissolved inorganic carbon pool was not derived from heterotrophic degradation of terrestrial organic carbon, but from degradation of autochthonous organic carbon, mineral dissolution, and atmospheric uptake. Optical characterization of dissolved organic matter revealed an autochthonous organic matter pool. CO₂ influx was correlated with autochthony, while efflux was correlated with total nitrogen and watershed wetland cover. Our findings suggest that CO₂ uptake by primary producers during blooms can contribute to continuous CO₂ influx for days to months. Conversely, eutrophic lakes in our study that were net sources of CO₂ to the atmosphere showed among the highest rates reported in the literature. These findings suggest that anthropogenic eutrophication has substantially altered biogeochemical processing of carbon on Earth.

 

Phytoplankton in extreme environments: importance and consequences of habitat permanency

Authors

Judit Padisák & Luigi Naselli-Flores

There is hardly any sunshine exposed surface on this Earth, be it water or terrain, which would not support some biota. Still, many habitats offer harsh conditions requiring specialized physiological adaptations to survive. These environments are referred to as extremes; often inhabited by extremophilic organisms. In this review, characteristic species and assemblage properties of phytoplankton inhabiting extreme environments (especially lakes and pools where planktic life is potentially possible and independently of their origin) in terms of alkalinity, acidity, DOC, salinity, temperature, light and mixing regime will be outlined. Lakes characterized by more than a single extreme are common (e.g. saline + alkaline; acidic + high DOC + high metal content + low light). At the edge of extremes (e.g. pH of 1; salinity over ~ 100–150 g l⁻¹) single species with appropriate physiological adaptation are selected and the phytoplankton is often dominated by a single species (monodominant) setting compositional diversity to zero. Under less extreme conditions permanent equilibria may persist; in many cases over several years in contrast to „average” lakes where equilibria are rare and ephemeral. Food webs depending on „extreme phytoplankton” are often atypical for example because the microbial loop is of prior importance or because birds are top predators.

 

Exploring the relative changes in dissolved organic matter for assessing the water quality of full-scale drinking water treatment plants using a fluorescence ratio approach

Authors

Tahir Maqbool, Yanling Qin, Quang Viet Ly, Jiaxing Zhang, Chengyue Li, Muhammad Bilal Asif, Zhenghua Zhang

This study aims to extend and demonstrate the application of fluorescence spectroscopy for monitoring the water quality of three differently operated full-scale drinking water treatment plants located in the Shenzhen city (China). A ratio of fluorescent dissolved organic matter (FDOM), which describes relative changes in humic-like to protein-like fluorescence, was used to explain mechanisms behind the physicochemical processes. The fluorescence components obtained through individual and combined parallel factor analysis (PARAFAC) modeling revealed the presence of humic-like (C1) and protein-like (C2) structures in the DOM. The C1/C2 ratio provided a direct relationship between the seasonal variations and DOM composition. Wet season generated DOM enriched with humic-like fluorescence, while dry season caused a higher release of protein-like fluorescence. The fluorescence ratio presented unique patterns of DOM in treatment trains. The chemical pretreatment and disinfection unit processes showed a higher tendency to remove the humic-like fluorescence. However, the C1/C2 ratio increased during physical treatment processes such as coagulation-precipitation and sand filtration, indicating preferential removal of protein-like fluorescence. The DOM composition in influent directly (R² = 0.77) influenced the relative intensities of fluorescence components in the treated water. Compared to the dry season, the wet season caused significant changes in DOM composition and produced treated water enriched with humic-like fluorescence. This fluorescence ratio offers an approach to explore the role of different treatment units and determine the factors affecting the composition of DOM in the surface water and drinking water treatment plants.

Formation of algal-derived nitrogenous disinfection by-products during chlorination and chloramination

Authors

X. Li, N.R.H. Rao, K.L. Linge, C.A. Joll, S. Khan, R.K. Henderson

Algal cells and algal organic matter (AOM) are a source of high dissolved organic carbon (DOC) and nitrogen (DON) concentrations. This poses a possible health risk due to their potential to form disinfection by-products (DBPs), some of which may be of health concern, after disinfection. While several studies have focussed on the formation of carbonaceous DBPs from AOM, only a few studies have focussed on the formation of nitrogen containing N-DBPs from AOM. Hence, the main aim of this study was to thoroughly investigate the N-DBP formation potential of the AOM from a species of cyanobacteria commonly found in natural waters, Microcystis aeruginosa. Three haloacetonitriles, two halonitromethanes, two haloacetamides, and eight N-nitrosamines were analysed by gas chromatography-mass spectrometry after chlorination and chloramination of the extracted AOM. To provide further insight into the influence of changing DON character on N-DBP formation potential, the AOM from three other species, Chlorella vulgaris, Dolichospermum circinale and Cylindrospermopsis raciborskii, were also tested. Dichloroacetonitrile (DCAN) was the DBP formed in the highest concentrations for both chlorination and chloramination of bulk AOM from all the species. Furthermore, during chlorination and chloramination, the high molecular weight fraction (>1 kDa) of AOM from M. aeruginosa had a greater DCAN formation potential (normalised to DOC or DON) than the AOM in the low molecular weight fraction (<1 kDa) of M. aeruginosa, regardless of growth stage. N-Nitrosamine formation from the bulk AOM of all species occurred only after chloramination. The molar concentration of N-nitrosodimethylamine (NDMA) was lower than the other N-nitrosamines detected. However, NDMA formation increased with culture age for all four species, in contrast to most other N-nitrosamines whose formation remained consistent or decreased with culture age. Overall, algal growth could result in elevated concentrations of N-DBPs due to the increasing concentrations of high molecular weight algal DON in the AOM. It is suggested that the AOM comprises precursors containing long C-chain amine (R₁-NH-R₂) or cyclic N-containing amine structures. Comparisons to previously measured N-DBP concentrations in drinking water suggest that the AOM from the algae and cyanobacteria examined in this study are not likely to be a major source of precursors for either DCAN or NDMA in real waters. However, AOM may present a major precursor source for other N-nitrosamines.

Sierra Nevada mountain lake microbial communities are structured by temperature, resources and geographic location

Authors

Marika A. Schulhof Andrew E. Allen Eric E. Allen Natalie Mladenov John P. McCrow Natalie T. Jones Jessica Blanton Hamanda B. Cavalheri Drishti Kaul Celia C. Symons Jonathan B. Shurin

Warming, eutrophication (nutrient fertilization) and brownification (increased loading of allochthonous organic matter) are three global trends impacting lake ecosystems. However, the independent and synergistic effects of resource addition and warming on autotrophic and heterotrophic microorganisms are largely unknown. In this study, we investigate the independent and interactive effects of temperature, dissolved organic carbon (DOC, both allochthonous and autochthonous) and nitrogen (N) supply, in addition to the effect of spatial variables, on the composition, richness, and evenness of prokaryotic and eukaryotic microbial communities in lakes across elevation and N deposition gradients in the Sierra Nevada mountains of California, USA. We found that both prokaryotic and eukaryotic communities are structured by temperature, terrestrial (allochthonous) DOC and latitude. Prokaryotic communities are also influenced by total and aquatic (autochthonous) DOC, while eukaryotic communities are also structured by nitrate. Additionally, increasing N availability was associated with reduced richness of prokaryotic communities, and both lower richness and evenness of eukaryotes. We did not detect any synergistic or antagonistic effects as there were no interactions among temperature and resource variables. Together, our results suggest that (a) organic and inorganic resources, temperature, and geographic location (based on latitude and longitude) independently influence lake microbial communities; and (b) increasing N supply due to atmospheric N deposition may reduce richness of both prokaryotic and eukaryotic microbes, probably by reducing niche dimensionality. Our study provides insight into abiotic processes structuring microbial communities across environmental gradients and their potential roles in material and energy fluxes within and between ecosystems.

 

Disentangling the drivers of Microcystis decomposition: Metabolic profile and co-occurrence of bacterial community

Authors

Shengnan Chen, Miaomiao Yan, Tinglin Huang, Hui Zhang, Kaiwen Liu, Xin Huang, Nan Li, Yutian Miao, Raju Sekar

In aquatic ecosystems, water microbial communities can trigger the outbreak or decline of cyanobacterial blooms. However, the microbiological drivers of Microcystis decomposition in reservoirs remain unclear. Here, we explored the bacterial community metabolic profile and co-occurrence dynamics during Microcystis decomposition. The results showed that the decomposition of Microcystis greatly altered the metabolic characteristics and composition of the water bacterial community. Significant variations in bacterial community composition were observed: the bacterial community was mainly dominated by Proteobacteria, Actinobacteria, Planctomycetes, and Bacteroidetes during Microcystis decomposition. Additionally, members of Exiguobacterium, Rhodobacter, and Stenotrophomonas significantly increased during the terminal stages. Dissolved organic matters (DOM) primarily composed of fulvic-like, humic acid-like, and tryptophan-like components, which varied distinctly during Microcystis decomposition. Additionally, the metabolic activity of the bacterial community showed a continuous decrease during Microcystis decomposition. Functional prediction showed a sharp increase in the cell communication and sensory systems of the bacterial communities from day 12 to day 22. Co-occurrence networks showed that bacteria responded significantly to variations in the dynamics of Microcystis decomposition through close interactions between each other. Redundancy analysis (RDA) indicated that Chlorophyll a, nitrate nitrogen (NO₃⁻-N), dissolved oxygen (DO), and dissolved organic carbon (DOC) were crucial drivers for shaping the bacterial community structure. Taken together, these findings highlight the dynamics of the water bacterial community during Microcystis decomposition from the perspective of metabolism and community composition, however, further studies are needed to understand the algal degradation process associated with bacteria.

Effects of pre, post, and simultaneous loading of natural organic matter on 2-methylisoborneol adsorption on superfine powdered activated carbon: Reversibility and external pore-blocking

Authors

Akiko Nakayama, Asuka Sakamoto, Taku Matsushita, Yoshihiko Matsui, Nobutaka Shirasaki

Three different natural organic matter (NOM)-loading methods were compared for the adsorptive removal of 2-methylisoborneol (MIB) by superfine powdered activated carbon (SPAC) and conventionally-sized powdered activated carbon (PAC). The three NOM-loading methods were: NOM adsorption followed by MIB (MIB adsorption on NOM-preloaded carbon), MIB adsorption followed by NOM (MIB adsorption on NOM post-loaded carbon), and simultaneous NOM and MIB loading (MIB adsorption on NOM-simultaneously loaded carbon). MIB removals were similar for the smaller-sized carbon (SPAC) at higher AC dosages and at lower initial NOM concentrations. The similar MIB removals indicate direct site competition between MIB and NOM with MIB adsorption reversibility (complete desorption of MIB by NOM). At lower AC doses, especially for PACs, and at higher initial NOM concentrations, the adsorption of MIBs depended on the sequence of MIB or NOM adsorption. MIB removal was lowest for the NOM-preloaded carbon, followed by NOM-simultaneously loaded carbon. The highest MIB removal was achieved by post-loading of NOM, indicating that the adsorption is irreversible. MIB adsorption on SPAC was more reversible than on PAC, although the pore size distributions of the two carbons were similar. The high degree of adsorption irreversibility for PAC compared with SPAC indicated that pore blocking occurs due to NOM loading at the PAC particle surface. Images of the external adsorption were obtained using isotope mapping and ¹⁵N-labeled effluent organic matter.

Two years of post-wildfire impacts on dissolved organic matter, nitrogen, and precursors of disinfection by-products in California stream waters

Authors

Habibullah Uzun, Randy A. Dahlgren, Christopher Olivares, Cagri Utku Erdem, Tanju Karanfil, Alex T. Chow

We investigated the effects of two California wildfires (Rocky and Wragg Fires, 2015) compared to an unburned reference watershed on water quality, dissolved organic matter (DOM), and precursors of disinfection by-products (DBPs) for two years’ post-fire. The two burned watersheds both experienced wildfires but differed in the proportion of burned watershed areas. Burned watersheds showed rapid water quality degradation from elevated levels of turbidity, color, and suspended solids, with greater degradation in the more extensively burned watershed. During the first year’s initial flushes, concentrations of dissolved organic carbon (DOC), dissolved organic nitrogen (DON), ammonium (NH₄⁺/NH₃), and specific ultraviolet absorbance (SUVA₂₅₄) were significantly higher (67 ± 40%, 418 ± 125%, 192 ± 120%, and 31 ± 17%, respectively) in the more extensively burned watershed compared to the reference watershed. These elevated values gradually declined and finally returned to levels like the reference watershed in the second year. Nitrate concentrations were near detection limits (0.01 mg-N/L) in the first year but showed a large increase in fire-impacted streams during the second rainy season, possibly due to delayed nitrification. Changes in DOM composition, especially during the initial storm events, indicated that fires can attenuate humic-like and soluble microbial by-product-like (SMP) DOM while increasing the proportion of fulvic-like, tryptophan-like, and tyrosine-like compounds. Elevated bromide (Br⁻) concentrations (up to 8.7 μM]) caused a shift in speciation of trihalomethanes (THMs) and haloacetic acids (HAAs) to brominated species for extended periods (up to 2 years). Wildfire also resulted in elevated concentrations of N-nitrosodimethylamine (NDMA) precursors. Such changes in THM, HAA, and NDMA precursors following wildfires pose a potential treatability challenge for drinking water treatment, but the effects are relatively short-term (≤1 year).