Microbial community successions and their dynamic functions during harmful cyanobacterial blooms in a freshwater lake

Authors

Hanyan Li, Mike Barber, Jingrang Lu, Ramesh Goel

The current study reports the community succession of different toxin and non-toxin producing cyanobacteria at different stages of cyanobacterial harmful algal blooms (CyanoHABs) and their connectivity with nitrogen and phosphorus cycles in a freshwater lake using an ecogenomics framework. Comprehensive high throughput DNA sequencing, water quality parameter measurements, and functional gene expressions over temporal and spatial scales were employed. Among the cyanobacterial community, the lake was initially dominated by Cyanobium during the months of May, June, and early July, and later primarily by Aphanizomenon and Dolichospermum depicting functional redundancy. Finally, Planktothrix appeared in late August and then the dominance switched to Planktothrix in September. Microcystis aeruginosa and Microcystis panniformis; two species responsible for cyanotoxin production, were also present in August and September, but in significantly smaller relative abundance. MC-LR (0.06–1.32 µg/L) and MC-RR (0.01–0.26 µg/L) were two major types of cyanotoxins detected. The presence of MC-LR and MC-RR were significantly correlated with the Microcystis-related genes (16SMic/mcyA/mcyG) and their expressions (r = 0.33 to 0.8, p < 0.05). The metabolic analyses further linked the presence of different cyanobacterial groups with distinct functions. The nitrogen metabolisms detected a relatively higher abundance of nitrite/nitrate reductase in early summer, indicating significant denitrification activity and the activation of N-fixation in the blooms dominated by Aphanizomenon/Dolichospermum (community richness) during nutrient-limited conditions. The phosphorus and carbohydrate metabolisms detected a trend to initiate a nutrient starvation alert and store nutrients from early summer, while utilizing the stored polyphosphate and carbohydrate (PPX and F6PPK) during the extreme ortho-P scarcity period, mostly in August or September. Specifically, the abundance of Aphanizomenon and Dolichospermum was positively correlated with the nitrogen-fixing nif gene and (p < 0.001) and the PPX enzyme for the stored polyphosphate utilization (r = 0.77, p < 0.001). Interestingly, the lake experienced a longer N-fixing period (2–3 months) before non-fixing cyanobacteria (Planktothrix) dominated the entire lake in late summer. The Provo Bay site, which is known to be nutrient-rich historically, had early episodes of filamentous cyanobacteria blooms compared to the rest of the lake.

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.

 

Grain size tunes microbial community assembly and nitrogen transformation activity under frequent hyporheic exchange: A column experiment

Authors

Yi Li, Jinxin Zhu, Longfei Wang, Yu Gao, Wenlong Zhang, Huanjun Zhang, Lihua Niu

Hyporheic zones (HZ) are hotspots for biogeochemical reactions where groundwater and surface water mix. River dam buildings and other hydrologic controls alter the sediment grain size distribution and modify the downstream hyporheic exchange, with cascading effects on geochemical and microbial processes in river corridors. In this lab-scale column experiment, the N transformations in HZ filled with sediments in different grain sizes were investigated with a focus on understanding the interplay among variational hydraulic connectivity, microbial community structure, functional potential under frequent groundwater−surface water exchange. Porosity was identified as the main driver determining bacterial community assembly in HZ sediments. Significant microbial zonation was observed along the columns and the degree of co-occurrence of bacterial communities in the Fine column was lower than that in the Coarse and Mix columns. The Coarse column allowed for almost 2.47 times the exchange flux relative to the Fine column, and generates the fastest DO consumption rate (−6.52 μg O₂/L·s). The enrichment of nitrifiers, i.e., Cytophagaceae and Bacillaceae and nitrification functional genes, i.e., amoA_AOA and amoA_AOB revealed the higher nitrification potential in column filled with coarse sediments. In comparison, the highest NH₄⁺ production rates (2.4 × 10⁻³ μg N/L·s) took place in Fine column. The higher abundancies of denitrifiers such as Comamonadaceae and Lysobacter and enrichment of functional genes of nirK and nirS interestingly suggested the elevated denitrification potential in Fine column in a more anaerobic environment. The results implied that variations in microbial functional potential and associated nitrogen transformation may occur in size-fractioned HZ to dynamic hyporheic exchange, which added new knowledge to the underlying biogeochemical and ecological processes in regulated river corridors.

Formation of N-nitrosodimethylamine precursors through the microbiological metabolism of nitrogenous substrates in water

Authors

Er Bei, Xiao Li, Fuhua Wu, Shixiang Li, Xinsheng He, Yufang Wang, Yu Qiu, Yu Wang, Chengkun Wang, Jun Wang, Xiaojian Zhang, Chao Chen

N-nitrosodimethylamine (NDMA) as one emerging disinfection by-product has been investigated globally since 1990s. However, its main precursors are still unclear. We found that NDMA formation potential (NDMAFP) of various water samples increased firstly and then decreased gradually during incubation with microorganism. We hypothesized that NDMA precursors could be produced through metabolism of nitrogenous components and then gradually be biodegraded. To verify this hypothesis, six amino acids (AAs), peptone and ammonium were separately incubated with microorganism and NDMAFP was measured regularly. The average molar yield of the substrates to NDMAFP were 60–200 × 10⁻⁶ for the AAs, 350 × 10⁻⁶ for peptone under aerobic condition. The extracellular fraction with molecular weight (MW) less than 1 k Dalton contributed the majority to NDMAFP in the peptone experiment, followed by that with MW between 10 k and 0.22 μm and the intracellular materials. Dimethylamine and methylamine were detected during the experiments but their contribution to NDMAFP is quite limited. The results indicate that the nitrosamine precursors may not be the direct metabolite of AAs or peptones but the excretion of living bacteria or the components in dead bacteria body. Our results inferred that AA metabolism may give an NDMAFP of 0.12 nmol/L (maximum) or 0.09 nmol/L (average) in water under aerobic condition. This estimation of NDMAFP from AA metabolism can account for 38% (maximum) or 27% (average) of the median NDMAFP in waters of China (0.32 nmol/L) reported before.

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.

 

Mitigating the global expansion of harmful cyanobacterial blooms: Moving targets in a human- and climatically-altered world

Authors

Hans W. Paerl, Malcolm A. Barnard

Cyanobacterial harmful algal blooms (CyanoHABs) are a major threat to human and environmental health. As global proliferation of CyanoHABs continues to increase in prevalence, intensity, and toxicity, it is important to identify and integrate the underlying causes and controls of blooms in order to develop effective short- and long-term mitigation strategies. Clearly, nutrient input reductions should receive high priority. Legacy effects of multi-decadal anthropogenic eutrophication have altered limnetic systems such that there has been a shift from exclusive phosphorus (P) limitation to nitrogen (N) limitation and N and P co-limitation. Additionally, climate change is driving CyanoHAB proliferation through increasing global temperatures and altered precipitation patterns, including more extreme rainfall events and protracted droughts. These scenarios have led to the “perfect storm scenario”; increases in pulsed nutrient loading events, followed by persistent low-flow, long water residence times, favoring bloom formation and proliferation. To meet the CyanoHAB mitigation challenge, we must: (1) Formulate watershed and airshed-specific N and P input reductions on a sliding scale to meet anthropogenic and climatic forcings. (2) Develop CyanoHAB management strategies that incorporate current and anticipated climatic changes and extremes. (3) Make nutrient management strategies compatible with other physical-chemical-biological mitigation approaches, such as altering freshwater flow and flushing, dredging, chemical applications, introduction of selective grazers, etc. (4) Target CyanoHAB toxin production and developing management approaches to reduce toxin production. (5) Develop broadly applicable long-term strategies that incorporate the above recommendations.

Role of algal accumulations on the partitioning between N2 production and dissimilatory nitrate reduction to ammonium in eutrophic lakes

Authors

Xingyu Jiang, Guang Gao, Lu Zhang, Xiangming Tang, Keqiang Shao, Yang Hu, Jian Cai

Cyanobacterial blooms change benthic nitrogen (N) cycling in eutrophic lake ecosystems by affecting organic carbon (OC) delivery and changing in nutrients availability. Denitrification, anaerobic ammonium oxidation (anammox), and dissimilatory nitrate reduction to ammonium (DNRA) are critical dissimilatory nitrate reduction pathways that determine N removal and N recycling in aquatic environments. A mechanistic understanding of the influence of algal accumulations on partitioning among these pathways is currently lacking. In the present study, a manipulative experiment in aquarium tanks was conducted to determine the response of dissimilatory nitrate reduction pathways to changes in algal biomass, and the interactive effects of OC and nitrate. Potential dinitrogen (N₂) production and DNRA rates, and related functional gene abundances were determined during incubation of 3–4 weeks. The results indicated that high algal biomass promoted DNRA but not N₂ production. The concentrations of dissolved organic carbon were the primary factor affecting DNRA rates. Low nitrate availability limited N₂ production rates in treatments with algal pellets and without nitrate addition. Meanwhile, the AOAamoA gene abundance was significantly correlated with the nrfA and nirS gene abundances, suggesting that coupled nitrification-denitrification/DNRA was prevalent. Partitioning between N₂ production and DNRA was positively correlated with the ratios of dissolved organic carbon to nitrate. Correspondingly, in Lake Taihu during summer to fall, the relatively high organic carbon/nitrate might favorably facilitate DNRA over denitrification, subsequently sustaining cyanobacterial blooms.

Nitrogen Stimulates Microcystis-Dominated Blooms More than Phosphorus in River Conditions That Favor Non-Nitrogen-Fixing Genera

Authors

Kyunghyun Kim, Hyunsaing Mun, Hyunjoo Shin, Sanghyun Park, Chungseok Yu, Jaehak Lee, Yumi Yoon, Hyeonsu Chung, Hyeonjeong Yun, Kyunglak Lee, Geonhee Jeong, Jin-a Oh, Injung Lee, Haejin Lee, Taewoo Kang, Hui Seong Ryu, Jonghwan Park, Yuna Shin, and Doughee Rhew

Despite the implementation of intensive phosphorus reduction measures, periodic outbreaks of cyanobacterial blooms in large rivers remain a problem in Korea, raising the need for more effective solutions to reduce their occurrence. This study sought to evaluate whether phosphorus or nitrogen limitation is an effective approach to control cyanobacterial (Microcystis) blooms in river conditions that favor this non-nitrogen-fixing genus. These conditions include nutrient enrichment, high water temperature, and thermal stratification during summer. Mesocosm bioassays were conducted to investigate the limiting factors for cyanobacterial blooms in a river reach where severe Microcystis blooms occur annually. We evaluated the effect of five different nitrogen (3, 6, 9, 12, and 15 mg/L) and phosphorus (0.01, 0.02, 0.05, 0.1, and 0.2 mg/L) concentrations on algae growth. The results indicate that nitrogen treatments stimulated cyanobacteria (mostly Microcystis aeruginosa) more than phosphorus. Interestingly, phosphorus additions did not stimulate cyanobacteria, although it did stimulate Chlorophyceae and Bacillariophyceae. We conclude that phosphorus reduction might have suppressed the growth of Chlorophyceae and Bacillariophyceae more than that of cyanobacteria; therefore, nitrogen or at least both nitrogen and phosphorus control appears more effective than phosphorus reductions alone for reducing cyanobacteria in river conditions that are favorable for non-nitrogen-fixing genera.

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).