Linking diatom sensitivity to herbicides to phylogeny: a step forward for biomonitoring?

Phylogeny has not yet been fully accepted in the field of ecotoxicology, despite studies demonstrating its potential for developing environmental biomonitoring tools, as it can provide an a priori assessment of the sensitivity of several indicator organisms. We therefore investigated the relationship between phylogeny and sensitivity to herbicides in freshwater diatom species. This study was performed on four photosystem II inhibitor herbicides (atrazine, terbutryn, diuron, and isoproturon) and 14 diatom species representative of Lake Geneva biofilm diversity. Using recent statistical tools provided by phylogenetics, we observed a strong phylogenetic signal for diatom sensitivity to herbicides. There was a major division in sensitivity to herbicides within the phylogenetic tree. The most sensitive species were mainly centrics and araphid diatoms (in this study, Thalassiosirales and Fragilariales), whereas the most resistant species were mainly pennates (in this study, Cymbellales, Naviculales, and Bacillariales). However, there was considerable variability in diatom sensitivity within the raphid clade, which could be explained by differences in trophic preferences (autotrophy or heterotrophy). These traits appeared to be complementary in explaining the differences in sensitivity observed at a refined phylogenetic level. Using phylogeny together with complementary traits, as trophic preferences, may help to predict the sensitivity of communities with a view to protecting their ecosystem.

[1]  Frédéric Rimet,et al.  Using diatom life-forms and ecological guilds to assess organic pollution and trophic level in rivers: a case study of rivers in south-eastern France , 2011, Hydrobiologia.

[2]  Rolf Altenburger,et al.  Predicting and observing responses of algal communities to photosystem ii‐herbicide exposure using pollution‐induced community tolerance and species‐sensitivity distributions , 2005, Environmental toxicology and chemistry.

[3]  T. Backhaus,et al.  Mixture toxicity from photosystem II inhibitors on microalgal community succession is predictable by concentration addition , 2010, Environmental toxicology and chemistry.

[4]  David G. Mann,et al.  Evolution of the diatoms: insights from fossil, biological and molecular data , 2006 .

[5]  H. Claustre,et al.  BOLIDOMONAS: A NEW GENUS WITH TWO SPECIES BELONGING TO A NEW ALGAL CLASS, THE BOLIDOPHYCEAE (HETEROKONTA) , 1999 .

[6]  F. Rimet,et al.  Biomonitoring river diatoms: Implications of taxonomic resolution , 2012 .

[7]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[8]  R. Gilliom Pesticides in U.S. streams and groundwater. , 2007, Environmental science & technology.

[9]  F. Zechman,et al.  USE OF RIBOSOMAL DNA INTERNAL TRANSCRIBED SPACERS FOR PHYLOGENETIC STUDIES IN DIATOMS 1 , 1994 .

[10]  L. Medlin,et al.  Evolution of the diatoms (Bacillariophyta). II. Nuclear-encoded small-subunit rRNA sequence comparisons confirm a paraphyletic origin for the centric diatoms. , 1996, Molecular biology and evolution.

[11]  V. Resh Multinational, Freshwater Biomonitoring Programs in the Developing World: Lessons Learned from African and Southeast Asian River Surveys , 2007, Environmental management.

[12]  O. Gascuel,et al.  SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. , 2010, Molecular biology and evolution.

[13]  H. Blanck,et al.  Multivariate patterns of algal sensitivity to chemicals in relation to phylogeny. , 1988, Ecotoxicology and environmental safety.

[14]  Ø. Moestrup,et al.  Phylogeny of the Bacillariaceae with emphasis on the genus Pseudo-nitzschia (Bacillariophyceae) based on partial LSU rDNA , 2002 .

[15]  Carola A. Schriever,et al.  The footprint of pesticide stress in communities--species traits reveal community effects of toxicants. , 2008, The Science of the total environment.

[16]  K. T. Kiss,et al.  Phylogeny of six naviculoid diatoms based on 18S rDNA sequences. , 2001, International journal of systematic and evolutionary microbiology.

[17]  A. Boudou,et al.  Aquatic ecotoxicology: from the ecosystem to the cellular and molecular levels. , 1997, Environmental health perspectives.

[18]  T. Backhaus,et al.  Predictability of the mixture toxicity of 12 similarly acting congeneric inhibitors of photosystem II in marine periphyton and epipsammon communities. , 2004, Aquatic toxicology.

[19]  R. Todeschini,et al.  QSAR approach for the selection of congeneric compounds with a similar toxicological mode of action. , 2001, Chemosphere.

[20]  A. Boudou,et al.  Effects of the phenylurea herbicide isoproturon on periphytic diatom communities in freshwater indoor microcosms. , 1996, Environmental pollution.

[21]  Michel Coste,et al.  Variations of periphytic diatom sensitivity to the herbicide diuron and relation to species distribution in a contamination gradient: implications for biomonitoring. , 2011, Journal of environmental monitoring : JEM.

[22]  M. Pagel Inferring the historical patterns of biological evolution , 1999, Nature.

[23]  D. Schluter,et al.  LIKELIHOOD OF ANCESTOR STATES IN ADAPTIVE RADIATION , 1997, Evolution; international journal of organic evolution.

[24]  Linda K. Medlin,et al.  Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision , 2004 .

[25]  D. Moreland,et al.  Interference of Herbicides with the Hill Reaction of Isolated Chloroplasts , 1962 .

[26]  R. Jeffree,et al.  Phylogenetic consistencies among chondrichthyan and teleost fishes in their bioaccumulation of multiple trace elements from seawater. , 2010, The Science of the total environment.

[27]  B. Siegfried,et al.  Comparative Sensitivity of Freshwater Algae to Atrazine , 2006, Bulletin of environmental contamination and toxicology.

[28]  M Coste,et al.  Sensitivity of freshwater periphytic diatoms to agricultural herbicides. , 2009, Aquatic toxicology.

[29]  Agnès Bouchez,et al.  Assessment of toxicity thresholds in aquatic environments: does benthic growth of diatoms affect their exposure and sensitivity to herbicides? , 2013, The Science of the total environment.

[30]  T. Reynoldson,et al.  Biomonitoring in North American Rivers: A Comparison of Methods Used for Benthic Macroinvertebrates in Canada and the United States , 2006 .

[31]  R. Jansen,et al.  A preliminary multi gene phylogeny of the diatoms (Bacillariophyta): Challenges for future research , 2010 .

[32]  V. Resh Which group is best? Attributes of different biological assemblages used in freshwater biomonitoring programs , 2008, Environmental monitoring and assessment.

[33]  W. Oettmeier,et al.  Herbicide resistance and supersensitivity in photosystem II , 1999, Cellular and Molecular Life Sciences CMLS.

[34]  B. Whitton,et al.  Comparative performance of benthic diatom indices used to assess river water quality , 1995, Hydrobiologia.

[35]  J. Sinkeldam,et al.  A coded checklist and ecological indicator values of freshwater diatoms from The Netherlands , 1994, Netherland Journal of Aquatic Ecology.

[36]  Maxim Teslenko,et al.  MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space , 2012, Systematic biology.

[37]  A. El Jay Effects of organic solvents and solvent-atrazine interactions on two algae, Chlorella vulgaris and Selenastrum capricornutum. , 1996, Archives of environmental contamination and toxicology.

[38]  A. Austin,et al.  Diatom Succession and Interaction in Littoral Periphyton and Plankton , 1973, Hydrobiologia.

[39]  ASSESSMENT of toxicity. , 1957, Monthly bulletin of the Ministry of Health and the Public Health Laboratory Service.

[40]  G. Hunt,et al.  Does extinction wield an axe or pruning shears? How interactions between phylogeny and ecology affect patterns of extinction , 2011, Paleobiology.

[41]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[42]  T. Christensen,et al.  The Diatoms. Biology and Morphology of the Genera , 1991 .

[43]  S. Lek,et al.  Using phylogenetic information to predict species tolerances to toxic chemicals , 2011 .

[44]  R. Lowe,et al.  22 – Benthic Algal Communities as Biological Monitors , 1996 .

[45]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[46]  Lucien Hoffmann,et al.  A preliminary phylogenetic analysis of the Cymbellales based on 18S rDNA gene sequencing , 2011 .

[47]  Pieter Vanormelingen,et al.  An Inordinate Fondness? The Number, Distributions, and Origins of Diatom Species , 2013, The Journal of eukaryotic microbiology.

[48]  Ary A. Hoffmann,et al.  Phylogenetic signals and ecotoxicological responses: potential implications for aquatic biomonitoring , 2011, Ecotoxicology.

[49]  F. Rimet,et al.  Next‐generation sequencing to inventory taxonomic diversity in eukaryotic communities: a test for freshwater diatoms , 2013, Molecular ecology resources.

[50]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[51]  P. Gramatica,et al.  Predicting the joint algal toxicity of multi-component s-triazine mixtures at low-effect concentrations of individual toxicants. , 2001, Aquatic toxicology.

[52]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[53]  J. Smol,et al.  USE OF ALGAE IN ENVIRONMENTAL ASSESSMENTS , 2003 .

[54]  F. Rimet,et al.  Influence of Herbicide Contamination on Diversity and Ecological Guilds of River Diatoms , 2013 .

[55]  T. Jombart,et al.  Putting phylogeny into the analysis of biological traits: a methodological approach. , 2010, Journal of theoretical biology.

[56]  T. Jombart,et al.  How to measure and test phylogenetic signal , 2012 .

[57]  J. Schaumburg,et al.  Macrophytes and phytobenthos as indicators of ecological status in German lakes — a contribution to the implementation of the water framework directive , 2004 .

[58]  R. Jansen,et al.  Status of the Pursuit of the Diatom Phylogeny: Are Traditional Views and New Molecular Paradigms Really That Different? , 2011 .

[59]  L. Medlin,et al.  A Review of the Evolution of the Diatoms from the Origin of the Lineage to Their Populations , 2011 .

[60]  D. Gallacher The application of rapid bioassessment techniques based on benthic macroinvertebrates in East Asian rivers (a review) , 2001 .

[61]  R. Relyea,et al.  Phylogeny meets ecotoxicology: evolutionary patterns of sensitivity to a common insecticide , 2012, Evolutionary applications.

[62]  Theodore Garland,et al.  Aquatic insect ecophysiological traits reveal phylogenetically based differences in dissolved cadmium susceptibility , 2008, Proceedings of the National Academy of Sciences.

[63]  Thibaut Jombart,et al.  Bioinformatics Applications Note Phylogenetics Adephylo: New Tools for Investigating the Phylogenetic Signal in Biological Traits , 2022 .

[64]  Elizabeth C. Ruck,et al.  Origin and evolution of the canal raphe system in diatoms. , 2011, Protist.

[65]  Frédéric Rimet,et al.  Recent views on river pollution and diatoms , 2012, Hydrobiologia.

[66]  H. Blanck,et al.  A phylogenetic approach to detect selection on the target site of the antifouling compound irgarol in tolerant periphyton communities. , 2009, Environmental microbiology.

[67]  E. Paradis Analysis of Phylogenetics and Evolution with R , 2006 .

[68]  Barbara R. Holland,et al.  Analysis of Phylogenetics and Evolution with R , 2007 .

[69]  Frédéric Rimet,et al.  Use of diatom life-forms and ecological guilds to assess pesticide contamination in rivers: Lotic mesocosm approaches , 2011 .

[70]  Sandrine Pavoine,et al.  Linking patterns in phylogeny, traits, abiotic variables and space: a novel approach to linking environmental filtering and plant community assembly , 2011 .

[71]  Campbell O. Webb,et al.  Picante: R tools for integrating phylogenies and ecology , 2010, Bioinform..

[72]  F. Rimet,et al.  Using Bioassays and Species Sensitivity Distributions to Assess Herbicide Toxicity towards Benthic Diatoms , 2012, PloS one.