Evaluating the Congruence Between DNA‐Based and Morphological
Total Page：16
File Type：pdf, Size：1020Kb
Limnol. Oceanogr. 9999, 2021, 1–20 © 2021 The Authors. Limnology and Oceanography published by Wiley Periodicals LLC on behalf of Association for the Sciences of Limnology and Oceanography. doi: 10.1002/lno.11856 Evaluating the congruence between DNA-based and morphological taxonomic approaches in water and sediment trap samples: Analyses of a 36-month time series from a temperate monomictic lake Joanna Gauthier ,1,2* David Walsh ,2,3 Daniel T. Selbie,4 Alyssa Bourgeois,1 Katherine Griffiths,1,2 Isabelle Domaizon,4,5 Irene Gregory-Eaves1,2 1Department of Biology, McGill University, Montreal, Quebec, Canada 2Groupe de Recherche Interuniversitaire en Limnologie (GRIL), Montreal, Quebec, Canada 3Department of Biology, Concordia University, Montreal, Quebec, Canada 4Fisheries and Oceans Canada, Pacific Region, Science Branch, Ecosystem Sciences Division, Cultus Lake Salmon Research Laboratory, Cultus Lake, British Columbia, Canada 5CARRTEL, INRAe, Université de Savoie Mont Blanc, Thonon-les-Bains, France Abstract Paleolimnological studies are central for identifying long-term changes, yet many studies rely on bioindicators that deposit detectable subfossils in sediments, such as diatoms and cladocerans. Emerging DNA-based approaches are expanding the taxonomic diversity that can be investigated. However, as sedimentary DNA-based approaches are expanding rapidly, calibration work is required to determine the advantages and limitations of these tech- niques. In this study, we assessed the congruence between morphological and DNA-based approaches applied to sediment trap samples for diatoms and crustaceans using both intracellular and extracellular DNA. We also evalu- ated which taxa are deposited in sediment traps from the water column to identify potential paleolimnological bioindicators of environmental variations. Based on 18S rRNA gene amplicons, we developed and analyzed a micro-eukaryotic, monthly time series that spanned 3 years and was comprised of paired water column and sedi- ment trap samples from Cultus Lake, British Columbia, Canada. Comparisons of assemblages derived from our genetic and morphological analyses using RV coefficients revealed significant correlations for diatoms, but weaker correlations for crustaceans. Intracellular DNA reads correlated more strongly with diatom morphology, while extracellular DNA reads correlated more strongly with crustacean morphology. Additional analyses of amplicon sequence variants shared between water and sediment trap samples revealed a wide diversity of taxa to study in paleolimnology, including Ciliophora, Dinoflagellata, Chytridiomycota, Chrysophyceae, and Cryptophyceae. Par- tial RDAs identified significant environmental predictors of these shared assemblages. Overall, our study demon- strates the effectiveness of DNA-based approaches to track community dynamics from sediment samples, an essential step for successful paleolimnological studies. Over the past century, anthropogenic activities and climate change (Smol 2008; Bennion et al. 2011). Paleolimnological time change have induced significant alterations to freshwater ecosys- series have been useful in evaluating the adequacy of manage- tems, with an intensification of stressors since the 1970s (Reid ment practices (Perga et al. 2010) and may inform future scenario et al. 2018). Paleolimnological records have played a central role development (Smol 2008; Gillson and Marchant 2014; Saulnier- in quantifying the rate and magnitude of past ecological dynam- Talbot 2016). Biological community changes in the sediment ics and have served to identify the major drivers of ecosystem record have relied mostly on the study of a small subset of aquatic taxa that deposit detectable subfossils including diatom valves (Battarbee et al. 2001), chrysophyte cysts and scales (Zeeb and *Correspondence: [email protected] Smol 2001) and cladoceran (Alric and Perga 2011) and chirono- mid remains (Walker 2001). However, many pelagic organisms This is an open access article under the terms of the Creative Commons fi Attribution-NonCommercial-NoDerivs License, which permits use and dis- do not preserve as visually identi able subfossils in the sediments tribution in any medium, provided the original work is properly cited, the (e.g., fungi, soft algae, rotifers, and copepods), yet may be useful fi use is non-commercial and no modi cations or adaptations are made. as bioindicators of environmental change. Additional Supporting Information may be found in the online version of Applying DNA-based approaches to lake sediments has the this article. potential to expand the taxonomic diversity that can be 1 Gauthier et al. Evaluating DNA-based methods in lake sediments targeted in paleolimnological studies, and to provide an protists, fungi, and larger multicellular organisms such as crus- opportunity to study functional genes (Domaizon tacean species. We refer to the pool of taxa identified through et al. 2017). Molecular approaches in paleolimnology have sequencing herein as micro-eukaryotes. Our specific aims were proven to be effective in reconstructing the histories of some (1) to evaluate the congruence of widely used bioindicator taxonomic groups such as cyanobacteria (Domaizon groups (diatom and crustaceans) between morphological and et al. 2013; Monchamp et al. 2016), diatoms (Epp et al. 2011; DNA approaches as well as between water and sediment trap Stoof-Leichsenring et al. 2014, 2020) and micro-eukaryotic samples, (2) to compare the micro-eukaryotic communities communities (Capo et al. 2016, 2017, 2019). However, only a identified from the amplification of the 18S rRNA gene from few studies have evaluated the congruence between morpho- DNA in the water column and in the sediment traps to iden- logical and DNA-based taxonomic approaches in sediments tify potential taxonomic groups for future paleolimnological (Stoof-Leichsenring et al. 2012, 2014, 2020; Dulias studies, and (3) to evaluate the efficiency of extracellular DNA et al. 2017). Preliminary results showed that DNA-based vs. intracellular DNA to detect taxa in sediment traps when approaches may uncover greater richness (Stoof-Leichsenring looking at diatom, crustacean and micro-eukaryotic assem- et al. 2012), and generally, these two approaches are consid- blages. Given that several studies have reported a significant ered complementary (Jørgensen et al. 2012; Dulias congruence between the assemblages observed in the water et al. 2017). Additionally, there is a need to evaluate the column and those recorded in lake sediments (Capo extent to which the biological signal from the water column et al. 2015; Winegardner et al. 2015; Monchamp et al. 2016), is captured in the sedimentary record when applying DNA- we hypothesize that analyses of sediment traps would track based approaches. Some promising initial studies include: similar dynamics to those reflected in the water column using (1) Capo et al. (2015) who detected 71% of phylogenetic similar taxonomic approaches (morphological or DNA). In units from the water column in the sediments and (2) Mon- addition, the few studies that have compared assemblages champ et al. (2016) who found that pelagic cyanobacteria based on sedimentary DNA and visual count approaches have identified morphologically over 30 years from water column detected significant coherence (Jørgensen et al. 2012; Stoof- sampleswerehighlycorrelatedwhencomparedtopaleo- Leichsenring et al. 2012; Monchamp et al. 2016). Accordingly, genetic time series of cyanobacteria. we hypothesize that the genetically and morphologically Sedimentary DNA can be archived either as intracellular derived estimates of taxonomic composition in the sediments (i.e., intact cells) or extracellular DNA, where extracellular would be significantly correlated. DNA can be adsorbed to the sediment matrix, thereby reduc- ing its degradability (Dell’Anno et al. 2002; Corinaldesi Methods et al. 2005; Dell’Anno and Danovaro 2005). In marine envi- ronments, extracellular DNA can represent >90% of the sedi- Site description ’ ’ mentary DNA pool (Dell’Anno et al. 2002; Dell’Anno and Cultus Lake (49 03.3 N; 121 59.0 W) is a monomictic and Danovaro 2005) and may be a significant fraction of the DNA oligo-mesotrophic lake located in the Lower Mainland of Brit- archived for many organisms. To our knowledge, only two ish Columbia (BC), Canada, at ~ 50 km east of the outer limit paleolimnological study have evaluated whether DNA from of the Greater Vancouver Regional District (Fig. 1a). The sur- 2 pelagic organisms is preserved as extracellular DNA in the sedi- face area of Cultus Lake is 6.3 km with mean and maximum ments (Vuillemin et al. 2017: bacteria; Pansu et al. 2021: depths of 31 and 44 m, respectively (Shortreed 2007). Cultus fl eukaryotes). Lake is a relatively fast- ushing lake with a water residence 2 Since the use of DNA-based approaches in paleolimnology time of ~ 1.8 yr. The lake watershed area is ~ 75 km with a is expanding rapidly, careful examination of the strengths and small proportion (~ 19%) in the United States. limitations of the approach is required. In this study, we gen- erated a sediment trap time series spanning 36 months in Sample collection order to advance our knowledge of how different components On a monthly basis from June 27th, 2014 to June 12th, of the pelagic communities may be detected from sedimentary 2017, water and sediment trap samples were collected and DNA by polymerase chain reaction (PCR)-based approaches. deployed at the offshore station where the Fisheries Although sediment