Water Research 185 (2020) 116292
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Water Research 185 (2020) 116292 Contents lists available at ScienceDirect Water Research journal homepage: www.elsevier.com/locate/watres Microbial community successions and their dynamic functions during harmful cyanobacterial blooms in a freshwater lake ∗ Hanyan Li a, Mike Barber a, Jingrang Lu b, Ramesh Goel a, a Civil & Environmental Engineering, University of Utah, 110 S. Central Campus Drive, 20 0 0 MCE, Salt Lake City, UT 84121, USA b United States Environmental Protection Agency, Office of Research and Development, Cincinnati, OH, USA a r t i c l e i n f o a b s t r a c t Article history: The current study reports the community succession of different toxin and non-toxin producing Received 25 June 2020 cyanobacteria at different stages of cyanobacterial harmful algal blooms (CyanoHABs) and their connectiv- Revised 8 August 2020 ity with nitrogen and phosphorus cycles in a freshwater lake using an ecogenomics framework. Compre- Accepted 10 August 2020 hensive high throughput DNA sequencing, water quality parameter measurements, and functional gene Available online 11 August 2020 expressions over temporal and spatial scales were employed. Among the cyanobacterial community, the Keywords: lake was initially dominated by Cyanobium during the months of May, June, and early July, and later Harmful algal blooms primarily by Aphanizomenon and Dolichospermum depicting functional redundancy. Finally, Planktothrix Cyanobium appeared in late August and then the dominance switched to Planktothrix in September. Microcystis aerug- Aphanizomenon inosa and Microcystis panniformis ; two species responsible for cyanotoxin production, were also present in Dolichospermum August and September, but in significantly smaller relative abundance. MC-LR (0.06–1.32 μg/L) and MC- Nitrogen fixation RR (0.01–0.26 μg/L) were two major types of cyanotoxins detected. The presence of MC-LR and MC-RR P Scavenging genes were significantly correlated with the Microcystis -related genes ( 16SMic / mcyA / mcyG ) and their expressions Cyanotoxins ( r = 0.33 to 0.8, p < 0.05). The metabolic analyses further linked the presence of different cyanobacte- rial 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 polyphos- phate 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 uti- lization ( 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. ©2020 Elsevier Ltd. All rights reserved. 1. Introduction Paerl et al., 2017 ). Early studies recognized P as the primary limiting nutrient in most lakes based on the stoichiometry of The input of excess nutrients, primarily nitrogen and phos- N and P in phytoplankton ( Schindler, 1977 ; Hecky and Kil- phorus, causes eutrophication in surface water bodies, lead- ham, 1988 ; Lewis and Wurtsbaugh, 2008 ). P addition-based bioas- ing to harmful algal blooms (HABs) in many freshwater lakes says have shown that P addition enhanced the growth of toxin- ( Heisler et al., 2008 ; Dodds et al., 2009 ; Keck and Lep- producing Microcystis ( Davis et al., 2009 ). However, subsequent ori, 2012 ; Drobac et al., 2013 ). Nitrogen (N) and phosphorus studies also found that N was often the limiting nutrient in (P) are two of the most important nutrients of concern, al- shallow eutrophic lakes, while the oligotrophic deep lake was though their relative contribution to eutrophication is always de- mostly P limited ( Downing and McCauley, 1992 ; Reynolds, 2006 ). batable ( Carpenter, 2005 ; Conley et al., 2009 ; Kolzau et al., 2014 ; A switch from spring P to summer N limitation has also been demonstrated in some locations ( Conley, 1999 ). Recent studies also recognized the dominance of cyanobacteria under low N/P ∗ Corresponding author. ratios ( Søndergaard et al., 2017 ; Isles et al., 2017 ). Generally, E-mail address: [email protected] (R. Goel). https://doi.org/10.1016/j.watres.2020.116292 0043-1354/© 2020 Elsevier Ltd. All rights reserved. 2 H. Li, M. Barber and J. Lu et al. / Water Research 185 (2020) 116292 an N-limitation condition could result from nitrate lost to het- ever, studies are still scarce for a whole-picture investigation into erotrophs (e.g., denitrifiers) via assimilation, denitrification and nutrient utilization pathways and toxin-producing functional genes other biochemical processes ( Allen et al., 2005 ; Chen et al., 2012 ; at the entire bacterial community level during HABs. Holmroos et al., 2012 ), while the levels of P were determined by The overall objective of this research was to take a holistic interactions between sediment and water column of seasonal hy- approach to illustrate the interdependency of CyanoHABs with drological processes ( Armon and Starosvetsky, 2015 ; Hogsett et al., several factors, including water quality parameters and genomic 2019 ; Ma et al., 2019 ). Nevertheless, none of the past efforts or re- contents in a freshwater peri-urban lake. This study fills an im- cent literature have denied the importance of nitrogen and phos- portant gap elated to the dynamics of P and N cycles during phorus in supporting surface water eutrophication ( Downing et al., cyanoHABs. Unlike a previous publication from this group on the 2001 ; Håkanson et al., 2007 ). ecology of cyanobacteria in Utah Lake ( Li et al., 2019 ), the objective With new species of cyanobacteria being identified, the also included studying N-fixing, P-regulating, and toxin-producing paradigm that surface water is either N limited or P limited is functional genes before the onset, during and after cyanoHABs fast changing because nutrient limitations also depend on which in addition to spatial and temporal variations in the abundances cyanobacterial species dominate the bloom ( Cottingham et al., of different cyanobacteria. The general N and P metabolic path- 2015 ). Under N stress conditions, many filamentous cyanobacte- ways and functions were predicted by Phylogenetic Investiga- ria (e.g., Aphanizomenon, Dolichospermum ) can conduct both nitro- tion of Communities by Reconstruction of Unobserved States (PI- gen fixation and photosynthesis by cell differentiation. It is well- CRUSt) ( Langille et al., 2013 ); the functional gene/gene expres- known that vegetative cells conduct primary productivity, whereas sions for nutrient scavenging ( nif/pst ) and microcystin-producing the specialized cells, heterocysts, perform nitrogen fixation by uti- ( mcy ) were precisely targeted by qPCR and Reverse-transcript qPCR lizing nitrogenases (encoded by nif genes; Schindler et al., 2008 ; ( Freeman et al., 1999 ). The main objectives of the study were to: Paerl, 2017 ). Additionally, N regulatory genes (e.g., ntrA, ntrC ) and (1) detect the microbial community shift and predict key func- PII signal transduction proteins are widely spread in bacteria that tional dynamics related to N and P; (2) study the dynamic behavior regulate the N assimilations under N starvations ( Hirschman et al., of nif genes, pst genes, and mcy genes during the CyanoHABs; (3) 1985 ; Herrero et al., 2004 ; Huergo et al., 2013 ). investigate the correlations among bacterial community presence, Similar to N systems, one of the commonly recognized strate- functions, and environmental factors. gies for bacteria to enhance phosphate assimilation is induc- ing the high-affinity inorganic phosphate (Pi) scavenging system- 2. Materials and methods Pho regulon ( Adams et al., 2008 ; Santos-Beneit, 2015 ), which in- cludes members having the high-affinity Pi transport systems (en- 2.1. Sampling sites coded by pst genes; Makino et al., 1988 ; Pitt et al., 2010 ), en- zymes polyphosphate kinase (PPK; Brown and Kornberg, 2004 ), Freshwater Utah Lake, which is located nearly 50 miles south of exopolyphosphatase ( PPX; Gomez-Garcia et al., 2003 ), and others. Salt Lake City, was considered as the model freshwater lake. Utah The P correlated metabolisms are even more complex to study, Lake is the largest natural freshwater lake in the western United as many P-containing compounds in cells are tightly linked with States, with a maximum length of 38.6 km and a maximum width carbohydrates assimilations ( Harke et al., 2012 ; Harke and Gob- of 20.9 km. As a shallow alkaline lake, it has an average depth ler, 2013 ) or the stringent conditions alert ( Abranches et al., 2009 ; of 3.0–3.4 m in open water during standard reservoir operating Santos-Beneit, 2015 ). It is reported that phosphate bioavailability conditions and has calcium-rich sediments. Utah Lake has experi- for diazotrophs was one of the constraint factors for nitrogen fix- enced frequent CyanoHABs in recent years, with the cyanobacteria ation rates as an interaction between N and