A large-scale assessment of lakes reveals a pervasive signal of land use on bacterial communities

Adrian R, O’Reilly CM, Zagarese H, Baines SB, Hessen DO, Keller W, et al. Lakes as sentinels of climate change. Limnol Oceanogr. 2009;54:2283–97.

PubMed  PubMed Central  Google Scholar 

Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, et al. Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr. 2009;54:2298–314.

Google Scholar 

Arbuckle KE, Downing JA. The influence of watershed land use on lake N: P in a predominantly agricultural landscape. Limnol Oceanogr. 2001;46:970–5.

Google Scholar 

Taranu ZE, Gregory-Eaves I. Quantifying relationships among phosphorus, agriculture, and lake depth at an inter-regional scale. Ecosystems. 2008;11:715–25.

Google Scholar 

Heisler J, Glibert PM, Burkholder JM, Anderson DM, Cochlan W, Dennison WC, et al. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae. 2008;8:3–13.

PubMed  PubMed Central  Google Scholar 

Scavia D, David Allan J, Arend KK, Bartell S, Beletsky D, Bosch NS, et al. Assessing and addressing the re-eutrophication of Lake Erie: Central basin hypoxia. J Gt Lakes Res. 2014;40:226–46.

Google Scholar 

Bastviken D, Cole J, Pace M, Tranvik L. Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Glob Biogeochem Cycles. 2004;18:1–12.

Google Scholar 

Novotny EV, Murphy D, Stefan HG. Increase of urban lake salinity by road deicing salt. Sci Total Environ. 2008;406:131–44.

PubMed  Google Scholar 

Dugan HA, Bartlett SL, Burke SM, Doubek JP, Krivak-Tetley FE, Skaff NK, et al. Salting our freshwater lakes. Proc Natl Acad Sci USA. 2017;114:4453–8.

PubMed  Google Scholar 

Hobbie SE, Finlay JC, Janke BD, Nidzgorski DA, Millet DB, Baker LA. Contrasting nitrogen and phosphorus budgets in urban watersheds and implications for managing urban water pollution. Proc Natl Acad Sci. 2017;114:4177–82.

PubMed  Google Scholar 

Shade A, Kent AD, Jones SE, Newton RJ, Triplett EW, McMahon KD. Interannual dynamics and phenology of bacterial communities in a eutrophic lake. Limnol Oceanogr. 2007;52:487–94.

Google Scholar 

Kara EL, Hanson PC, Hu YH, Winslow L, McMahon KD. A decade of seasonal dynamics and co-occurrences within freshwater bacterioplankton communities from eutrophic Lake Mendota, WI, USA. ISME J. 2013;7:680–4.

PubMed  Google Scholar 

Marmen S, Blank L, Al-Ashhab A, Malik A, Ganzert L, Lalzar M, et al. The role of land use types and water chemical properties in structuring the microbiome of a connected lake system. Front Microbiol. 2020;11:1–16.

Google Scholar 

Environment Canada Whole organism responses and intersex severity in rainbow darter (Etheostoma caeruleum) following exposures to municipal wastewater in the Grand River basin, ON, Canada. Part A, Municipal Water Use Rep. 2011;159:2011–301.

Google Scholar 

Huot Y, Brown CA, Potvin G, Antoniades D, Baulch HM, Beisner BE, et al. The NSERC Canadian Lake Pulse Network: a national assessment of lake health providing science for water management in a changing climate. Sci Total Environ. 2019;695:133668.

PubMed  Google Scholar 

Lu Y, Wang R, Zhang Y, Su H, Wang P, Jenkins A, et al. Ecosystem health towards sustainability. Ecosyst Heal Sustain. 2015;1:1–15.

Google Scholar 

Hering D, Borja A, Carvalho L, Feld CK. Assessment and recovery of European water bodies: Key messages from the WISER project. Hydrobiologia 2013;704:1–9.

Google Scholar 

U.S. Environmental Protection Agency. National Lake Assessment: a collaborative survey of the Nation’s Lakes. Washington, DC: EPA 841-R-09-001; 2009.

Ecological Stratification Working Group. A national ecological framework for Canada. Urbana-Champaign, Illinois: Ecological Stratification Working Group; 1996.

Glaz P, Gagné JP, Archambault P, Sirois P, Nozais C. Impact of forest harvesting on water quality and fluorescence characteristics of dissolved organic matter in eastern Canadian Boreal Shield lakes in summer. Biogeosciences. 2015;12:6999–7011.

Google Scholar 

Patton C, Kryskalla J. Methods of analysis by the U.S. Geological Survey National Water Quality Laboratory—evaluation of alakline digestion as an alternative to kjedahl digestion for determination of total and dissolved nitrogen and phosphorous. Denver, Colorado: Water-Resources Investigations Report 03; 2003.

U.S. Environmental Protection Agency. Method 200.7: determination of metals and trace elements in water and wastes by inductively coupled plasma-atomic emission spectrometry. Cincinatti, Ohio: U.S. Environmental Protection Agency; 1994.

U.S. Environmental Protection Agency. Method 300.1: determination of inorganic anions in drinking water by ion chromatography. Cincinatti, Ohio; 1997.

Wu Y. Barcode Demultiplex for Illumina I1, R1, R2 fastq.gz files. 2014.

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10.

Google Scholar 

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.

PubMed  PubMed Central  Google Scholar 

Rohwer RR, Hamilton JJ, Newton RJ, McMahon KD. TaxAss: leveraging a custom freshwater database achieves fine-scale taxonomic resolution. mSphere. 2018;3:1–14.

Google Scholar 

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6.

Google Scholar 

McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.

PubMed  PubMed Central  Google Scholar 

Price MN, Dehal PS, Arkin AP. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.

PubMed  PubMed Central  Google Scholar 

Dray S, Dufour A-B. The ade4 Package: implementing the duality diagram for ecologists. J Stat Softw. 2007;22:1–20.

Google Scholar 

Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D, et al. Vegan: community ecology package. 2016. https://cran.r-project.org; https://github.com/vegandevs/vegan.

Hair J, Tatham R, Anderson R, Black W. Multivariate data analysis. 5th ed. London: Prentice-Hall; 1998.

Google Scholar 

R Development Core Team T. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2009.

Google Scholar 

Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team T. nlme: linear and nonlinear mixed effect models. R package version. 3.1-141; 2019.

Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–51.

Google Scholar 

Rosseel Y. Lavaan: an R package for structural equation modeling. J Stat Softw. 2012;48:1–37.

Google Scholar 

Albanese D, Filosi M, Visintainer R, Riccadonna S, Jurman G, Furlanello C. Minerva and minepy: a C engine for the MINE suite and its R, Python and MATLAB wrappers. Bioinformatics. 2013;29:407–8.

PubMed  Google Scholar 

Kurtz ZD, Müller CL, Miraldi ER, Littman DR, Blaser MJ, Bonneau RA. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol. 2015;11:e1004226.

PubMed  PubMed Central  Google Scholar 

Banerjee S, Walder F, Büchi L, Meyer M, Held AY, Gattinger A, et al. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 2019;13:1722–36.

PubMed  PubMed Central  Google Scholar 

Barberán A, Bates ST, Casamayor EO, Fierer N. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 2012;6:343–51.

PubMed  Google Scholar 

Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, et al. Quantifying community assembly processes and identifying features that impose them. ISME J. 2013;7:2069–79.

PubMed  PubMed Central  Google Scholar 

Benlloch S, López-López A, Casamayor EO, Øvreås L, Goddard V, Daae FL, et al. Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol. 2002;4:349–60.

PubMed  Google Scholar 

Abed RMM, Kohls K, De Beer D. Effect of salinity changes on the bacterial diversity, photosynthesis and oxygen consumption of cyanobacterial mats from an intertidal flat of the Arabian Gulf. Environ Microbiol. 2007;9:1384–92.

PubMed  Google Scholar 

Lozupone CA, Knight R. Global patterns in bacterial diversity. Proc Natl Acad Sci USA. 2007;104:11436–40.

PubMed  Google Scholar 

Wu QL, Zwart G, Schauer M, Kamst-Van Agterveld MP, Hahn MW. Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Appl Environ Microbiol. 2006;72:5478–85.

PubMed  PubMed Central  Google Scholar 

Wang J, Yang D, Zhang Y, Shen J, van der Gast C, Hahn MW, et al. Do patterns of bacterial diversity along salinity gradients differ from those observed for macroorganisms? PLoS ONE. 2011;6:e27597.

PubMed  PubMed Central  Google Scholar 

Kelly VR, Lovett GM, Weathers KC, Findlay SEG, Strayer DL, Burns DJ, et al. Long-term sodium chloride retention in a rural watershed: legacy effects of road salt on streamwater concentration. Environ Sci Technol. 2008;42:410–5.

PubMed  Google Scholar 

Corsi SR, Graczyk DJ, Geis SW, Booth NL, Richards KD. A fresh look at road salt: aquatic toxicity and water-quality impacts on local, regional, and national scales. Environ Sci Technol. 2010;44:7376–82.

PubMed  PubMed Central  Google Scholar 

Levine SN, Schindler DW. Influence of nitrogen to phosphorus supply ratios and physicochemical conditions on cyanobacteria and phytoplankton species composition in the Experimental Lakes Area, Canada. Can J Fish Aquat Sci. 1999;56:451–66.

Google Scholar 

Stockner JG, Shortreed KS. Response of Anabaena and Synechococcus to manipulation of nitrogen: phosphorus ratios in a lake fertilization experiment. Limnol Oceanogr. 1988;33:1348–61.

Google Scholar 

Thad Scott J, McCarthys MJ. Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnol Oceanogr. 2010;55:1265–70.

Google Scholar 

Håkanson L, Blenckner T, Bryhn AC, Hellström SS. The influence of calcium on the chlorophyll-phosphorus relationship and lake Secchi depths. Hydrobiologia. 2005;537:111–23.

Google Scholar 

Eiler A, Heinrich F, Bertilsson S. Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J. 2012;6:330–42.

PubMed  Google Scholar 

Peura S, Bertilsson S, Jones RI, Eiler A. Resistant microbial cooccurrence patterns inferred by network topology. Appl Environ Microbiol. 2015;81:2090–7.

PubMed  PubMed Central  Google Scholar 

Logares R, Tesson SVM, Canbäck B, Pontarp M, Hedlund K, Rengefors K. Contrasting prevalence of selection and drift in the community structuring of bacteria and microbial eukaryotes. Environ Microbiol. 2018;20:2231–40.

PubMed  Google Scholar 

Lindström ES, Kamst-Van Agterveld MP, Zwart G. Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol. 2005;71:8201–6.

PubMed  PubMed Central  Google Scholar 

Lauber CL, Hamady M, Knight R, Fierer N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol. 2009;75:5111–20.

PubMed  PubMed Central  Google Scholar 

Xiong J, Liu Y, Lin X, Zhang H, Zeng J, Hou J, et al. Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol. 2012;14:2457–66.

PubMed  PubMed Central  Google Scholar 

Findlay DL, Kasian SEM. Phytoplankton community responses to acidification of lake 223, experimental lakes area, northwestern Ontario. Water Air Soil Pollut. 1986;30:719–26.

Google Scholar 

Findlay DL, Kasian SEM. The effect of incremental pH recovery on the Lake 223 phytoplankton community. Can J Fish Aquat Sci. 1996;53:856–64.

Google Scholar 

Maberly SC. Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshw Biol. 2008;35:579–98.

Google Scholar 

Tong Y, Lin G, Ke X, Liu F, Zhu G, Gao G, et al. Comparison of microbial community between two shallow freshwater lakes in middle Yangtze basin, East China. Chemosphere. 2005;60:85–92.

PubMed  Google Scholar 

Romina Schiaffino M, Unrein F, Gasol JM, Massana R, Balagué V, Izaguirre I. Bacterial community structure in a latitudinal gradient of lakes: the roles of spatial versus environmental factors. Freshw Biol. 2011;56:1973–91.

Google Scholar 

Zeng J, Yang L, Li J, Liang Y, Xiao L, Jiang L, et al. Vertical distribution of bacterial community structure in the sediments of two eutrophic lakes revealed by denaturing gradient gel electrophoresis (DGGE) and multivariate analysis techniques. World J Microbiol Biotechnol. 2009;25:225–33.

Google Scholar 

Canfield DE, Bachmann RW. Prediction of total phosphorus concentrations, chlorophyll a, and Secchi depths in natural and artificial lakes. Can J Fish Aquat Sci. 1981;38:414–23.

Google Scholar 

Meeuwig JJ, Peters RH. Circumventing phosphorus in lake management: a comparison of chlorophyll a predictions from land-use and phosphorus-loading models. Can J Fish Aquat Sci. 1996;53:1795–806.

Google Scholar 

Yang L, Lei K, Meng W, Fu G, Yan W. Temporal and spatial changes in nutrients and chlorophyll-α in a shallow lake, Lake Chaohu, China: an 11-year investigation. J Environ Sci (China). 2013;25:1117–23.

Google Scholar 

Kraemer SA, Soucy JPR, Kassen R. Antagonistic interactions of soil pseudomonads are structured in time. FEMS Microbiol Ecol. 2017;93:1–9.

Google Scholar