Assessing the ecological quality status of the highly polluted Bagnoli area (Tyrrhenian Sea, Italy) using foraminiferal eDNA metabarcoding

Cavaliere, M.; Angeles, Inès Barrenechea; Montresor, Marina; Bucci, Carla; Brocani, L.; Balassi, Eszter; Margiotta, Francesca; Francescangeli, Fabio; Bouchet, Vincent M. P.; Pawłowski, Jan; Frontalini, Fabrizio

doi:10.1016/j.scitotenv.2021.147871

Cited by 33 publications

(13 citation statements)

References 64 publications

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“…Metabarcoding methods have been used to identify foraminiferal community composition in water (Morard et al, 2018) and sediment samples (Frontalini et al, 2020;Li et al, 2020;Cavaliere et al, 2021). A recent study, however, unraveled extreme variations in the number of SSU rRNA gene copies in the genome of planktonic foraminifera (Milivojević et al, 2021).…”

Section: Beyond Species Identificationmentioning

confidence: 99%

Mitochondrial Cytochrome Oxidase Subunit 1: A Promising Molecular Marker for Species Identification in Foraminifera

et al. 2022

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Traditional morphological methods for species identification are highly time consuming, especially for small organisms, such as Foraminifera, a group of shell-building microbial eukaryotes. To analyze large amounts of samples more efficiently, species identification methods have extended to molecular tools in the last few decades. Although a wide range of phyla have good markers available, for Foraminifera only one hypervariable marker from the ribosomal region (18S) is widely used. Recently a new mitochondrial marker cytochrome oxidase subunit 1 (COI) has been sequenced. Here we investigate whether this marker has a higher potential for species identification compared to the ribosomal marker. We explore the genetic variability of both the 18S and COI markers in 22 benthic foraminiferal morphospecies (orders Miliolida and Rotaliida). Using single-cell DNA, the genetic variability within specimens (intra) and between specimens (inter) of each species was assessed using next-generation sequencing. Amplification success rate was twice as high for COI (151/200 specimens) than for 18S (73/200 specimens). The COI marker showed greatly decreased intra- and inter-specimen variability compared to 18S in six out of seven selected species. The 18S phylogenetic reconstruction fails to adequately cluster multiple species together in contrast to COI. Additionally, the COI marker helped recognize misclassified specimens difficult to morphologically identify to the species level. Integrative taxonomy, combining morphological and molecular characteristics, provides a robust picture of the foraminiferal species diversity. Finally, we suggest the use of a set of sequences (two or more) to describe species showing intra-genomic variability additionally to using multiple markers. Our findings highlight the potential of the newly discovered mitochondrial marker for molecular species identification and metabarcoding purposes.

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Section: Beyond Species Identificationmentioning

confidence: 99%

Mitochondrial Cytochrome Oxidase Subunit 1: A Promising Molecular Marker for Species Identification in Foraminifera

et al. 2022

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“…In foraminiferal morphospecies' assemblages, decreasing diversity is commonly associated with naturally‐ or pollution‐stressed conditions (Alve, 1995; Murray, 2006). The same was found for eDNA and eRNA diversity (i.e., taxonomic richness, Shannon diversity) comparing anthropogenically stressed environments to unstressed sites (e.g., fish‐farming in Pawlowski, Esling, et al, 2014; Pochon et al, 2015; gas and oil exploitation in Laroche et al, 2016; Laroche et al, 2018; Cordier, Frontalini, et al, 2019; Frontalini et al, 2020; industry in Cavaliere et al, 2021). Similarly, our foraminiferal eDNA diversity was comparable to previous morphology‐based studies, particularly in taxon richness of mineralized species (Choquel et al, 2021; Gustafsson & Nordberg, 1999, 2000, 2001), but not in terms of species' presence.…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, in a morphology‐based study of the saltwater Lake Grevelingen, Netherlands, extirpation of foraminiferal populations was only observed after 1–2 months of surface‐sediment anoxia whereas shorter low‐oxygen periods only affected abundances (Richirt et al, 2020). The validity of sequence abundance in eDNA metabarcoding reflecting species abundance is under active discussion (Frontalini et al, 2020; Weber & Pawlowski, 2013), although some studies showed congruence for dominant morpho‐ and molecular assemblage components (Cavaliere et al, 2021; Pawlowski, Esling, et al, 2014). Factors postulated to affect read abundance include biological biases, such as specimen biovolume, gene copy number, or divergence in primer regions, as well as amplification or sequencing artifacts (André et al, 2014; Elbrecht et al, 2017; Pawlowski, Esling, et al, 2014; Weber & Pawlowski, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Advantages include fast processing, potential of re‐analysis, and higher taxonomic resolution than achieved by conventional, observation‐based techniques (e.g., review by Pawlowski et al, 2022). To date, foraminiferal eDNA studies focused on the deep sea (abyssal to hadal depths: Cordier, Frontalini, et al, 2019; abyssal regions: Lejzerowicz et al, 2021) and, more recently, polluted areas adjacent to offshore fossil‐fuel drilling sites (Frontalini et al, 2020; Laroche et al, 2018; Mauffrey et al, 2021), fish farms (Pawlowski et al, 2016; Pawlowski, Esling, et al, 2014), and former steel mills (Cavaliere et al, 2021). However, impacts of other anthropogenic activities, such as the increased prevalence of oxygen‐deficient seawater, have rarely been assessed by metabarcoding approaches (Langlet et al, 2013), and studies focusing on natural variability are lacking particularly in near‐coast environments.…”

Section: Introductionmentioning

confidence: 99%

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Through the eDNA looking glass: Responses of fjord benthic foraminiferal communities to contrasting environmental conditions

Brinkmann

Schweizer

Quinchard

et al. 2023

J Eukaryotic Microbiology

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The health of coastal marine environments is severely declining with global changes. Proxies, such as those based on microeukaryote communities, can record biodiversity and ecosystem responses. However, conventional studies rely on microscopic observations of limited taxonomic range and size fraction, missing putatively ecologically informative community components. Here, we tested molecular tools to survey foraminiferal biodiversity in a fjord system (Sweden) on spatial and temporal scales: Alpha and beta diversity responses to natural and anthropogenic environmental trends were assessed and variability of foraminiferal environmental DNA (eDNA) compared to morphology‐based data. The identification of eDNA‐obtained taxonomic units was aided by single‐cell barcoding. Our study revealed wide diversity, including typical morphospecies recognized in the fjords, and so‐far unrecognized taxa. DNA extraction method impacted community composition outputs significantly. DNA extractions of 10 g sediment more reliably represented present diversity than of 0.5‐g samples and, thus, are preferred for environmental assessments in this region. Alpha‐ and beta diversity of 10‐g extracts correlated with bottom‐water salinity similar to morpho‐assemblage diversity changes. Sub‐annual environmental variability resolved only partially, indicating damped sensitivity of foraminiferal communities on short timescales using established metabarcoding techniques. Systematically addressing the current limitations of morphology‐based and metabarcoding studies may strongly improve future biodiversity and environmental assessments.

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“…They are based either on their diversity i.e., the exp(H bc ) [45] or on the species-specific response to total organic carbon content i.e., Foram-AMBI [41,46,47], TSI-Med [48] and Foram Stress Index [49]. These indices were successfully applied to assess the health of benthic habitats in the Mediterranean Sea [31,37,41,[48][49][50][51][52][53][54]. However, benthic foraminifera are not yet acknowledged as a biological quality element for the implementation of the WFD and MSFD.…”

Section: Introductionmentioning

confidence: 99%

Distribution Patterns of Benthic Foraminifera in Fish Farming Areas (Corsica, France): Implications for the Implementation of Biotic Indices in Biomonitoring Studies

Dubois

Barras

Pavard

et al. 2021

Water

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Corsican marine aquaculture is one of the highest contributors of fish production in France, which may result in environmental perturbations caused by organic matter (OM) accumulation under fish farms and impacting natural communities. This study aimed to (1) characterise the environmental conditions at two different fish farms, (2) monitor the response of benthic foraminiferal species to this activity, and (3) assess the accuracy of existing foraminiferal biotic indices. In 2017, sea floor sediment was sampled in transects from two Corsican fish farms for living foraminiferal and sedimentary analyses. Four indices were calculated and compared: exp(H′bc), Foram-AMBI, Foram Stress Index and TSI-Med. A significant increase in total organic carbon (TOC) has been shown, mainly below the fish cages. Communities were characterized by a shift from high density, opportunistic and tolerant species under the cages to lower densities and more sensitive species further away. According to their distribution patterns along the TOC gradient, we propose to update the ecological group classification of seven species to improve Foram-AMBI’s accuracy and sensitivity: Triloculina oblonga and Quinqueloculina lamarckiana to Ecological Group (EG) I; Rosalina bradyi to EGIII; and Bolivina dilatata, Bulimina aculeata and Quinqueloculina stalkeri to EGIV. We recommend prioritising the use of TSI-Med and Foram-AMBI with the updated list to assess ecological quality in coastal waters of the Mediterranean Sea.

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Assessing the ecological quality status of the highly polluted Bagnoli area (Tyrrhenian Sea, Italy) using foraminiferal eDNA metabarcoding

Cited by 33 publications

References 64 publications

Mitochondrial Cytochrome Oxidase Subunit 1: A Promising Molecular Marker for Species Identification in Foraminifera

Mitochondrial Cytochrome Oxidase Subunit 1: A Promising Molecular Marker for Species Identification in Foraminifera

Through the eDNA looking glass: Responses of fjord benthic foraminiferal communities to contrasting environmental conditions

Distribution Patterns of Benthic Foraminifera in Fish Farming Areas (Corsica, France): Implications for the Implementation of Biotic Indices in Biomonitoring Studies

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