Assessing the effect of mercury pollution on cultured benthic foraminifera community using morphological and eDNA metabarcoding approaches

none14sìMercury (Hg) is a highly toxic element for living organisms and is known to bioaccumulate and biomagnify. Here, we analyze the response of benthic foraminifera communities cultured in mesocosm and exposed to different concentrations of Hg. Standard morphological analyses and environmental DNA metabarcoding show evidence that Hg pollution has detrimental effects on benthic foraminifera. The molecular analysis provides a more complete view of foraminiferal communities including the soft-walled single-chambered monothalamiids and small-sized hard-shelled rotaliids and textulariids than the morphological one. Among these taxa that are typically overlooked in morphological studies we found potential bioindicators of Hg pollution. The mesocosm approach proves to be an effective method to study benthic foraminiferal responses to various types and concentrations of pollutants over time. This study further supports foraminiferal metabarcoding as a complementary and/or alternative method to standard biomonitoring program based on the morphological identification of species communities.openFrontalini, Fabrizio; Greco, Mattia; Di Bella, Letizia; Lejzerowicz, Franck; Reo, Emanuela; Caruso, Antonio; Cosentino, Claudia; Maccotta, Antonella; Scopelliti, Giovanna; Nardelli, Maria Pia; Losada, Maria Teresa; Armynot du Châtelet, Eric; Coccioni, Rodolfo; Pawlowski, JanFrontalini, Fabrizio; Greco, Mattia; Di Bella, Letizia; Lejzerowicz, Franck; Reo, Emanuela; Caruso, Antonio; Cosentino, Claudia; Maccotta, Antonella; Scopelliti, Giovanna; Nardelli, Maria Pia; Losada, Maria Teresa; Armynot du Châtelet, Eric; Coccioni, Rodolfo; Pawlowski, Ja

Foraminiferal survival after long-term in situ experimentally induced anoxia

Anoxia was successfully induced in four benthic chambers installed at 24 m depth on the northern Adriatic seafloor from 9 days to 10 months. To accurately determine whether benthic foraminifera can survive experimentally induced prolonged anoxia, the CellTrackerTM Green method was applied and calcareous and agglutinated foraminifera were analyzed. Numerous individuals were found living at all sampling times and at all sampling depths (to 5 cm), supported by a ribosomal RNA analysis that revealed that certain benthic foraminifera were active after 10 months of anoxia. The results show that benthic foraminifera can survive up to 10 months of anoxia with co-occurring hydrogen sulfides. However, foraminiferal standing stocks decrease with sampling time in an irregular manner. A large difference in standing stock between two cores sampled under initial conditions indicates the presence of a large spatial heterogeneity of the foraminiferal faunas. An unexpected increase in standing stocks after one month is tentatively interpreted as a reaction to increased food availability due to the massive mortality of infaunal macrofaunal organisms. After this, standing stocks decrease again in cores sampled after 2 months of anoxia to then attain a minimum in the cores sampled after 10 months. We speculate that the trend of overall decrease of standing stocks is not due to the adverse effects of anoxia and hydrogen sulfides but rather due to a continuous diminution of labile organic matter

Patterns of eukaryotic diversity from the surface to the deep-ocean sediment

Remote deep-ocean sediment (DOS) ecosystems are among the least explored biomes on Earth. Genomic assessments of their biodiversity have failed to separate indigenous benthic organisms from sinking plankton. Here, we compare global-scale eukaryotic DNA metabarcoding datasets (18S-V9) from abyssal and lower bathyal surficial sediments and euphotic and aphotic ocean pelagic layers to distinguish plankton from benthic diversity in sediment material. Based on 1685 samples collected throughout the world ocean, we show that DOS diversity is at least threefold that in pelagic realms, with nearly two-thirds represented by abundant yet unknown eukaryotes. These benthic communities are spatially structured by ocean basins and particulate organic carbon (POC) flux from the upper ocean. Plankton DNA reaching the DOS originates from abundant species, with maximal deposition at high latitudes. Its seafloor DNA signature predicts variations in POC export from the surface and reveals previously overlooked taxa that may drive the biological carbon pump

Planktonic foraminifera-derived environmental DNA extracted from abyssal sediments preserves patterns of plankton macroecology

The study was supported by Swiss National Science Foundation grants 31003A-140766 and 313003A-159709 and by the DFG Research Centre/Cluster of Excellence “The Ocean in the Earth System”.Deep-sea sediments constitute a unique archive of ocean change, fueled by a permanent rain of mineral and organic remains from the surface ocean. Until now, paleo-ecological analyses of this archive have been mostly based on information from taxa leaving fossils. In theory, environmental DNA (eDNA) in the sediment has the potential to provide information on non-fossilized taxa, allowing more comprehensive interpretations of the fossil record. Yet, the process controlling the transport and deposition of eDNA onto the sediment and the extent to which it preserves the features of past oceanic biota remains unknown. Planktonic foraminifera are the ideal taxa to allow an assessment of the eDNA signal modification during deposition because their fossils are well preserved in the sediment and their morphological taxonomy is documented by DNA barcodes. Specifically, we re-analyze foraminiferal-specific metabarcodes from 31 deep-sea sediment samples, which were shown to contain a small fraction of sequences from planktonic foraminifera. We confirm that the largest portion of the metabarcode originates from benthic bottom-dwelling foraminifera, representing the in situ community, but a small portion (< 10 %) of the metabarcodes can be unambiguously assigned to planktonic taxa. These organisms live exclusively in the surface ocean and the recovered barcodes thus represent an allochthonous component deposited with the rain of organic remains from the surface ocean. We take advantage of the planktonic foraminifera portion of the metabarcodes to establish to what extent the structure of the surface ocean biota is preserved in sedimentary eDNA. We show that planktonic foraminifera DNA is preserved in a range of marine sediment types, the composition of the recovered eDNA metabarcode is replicable and that both the similarity structure and the diversity pattern are preserved. Our results suggest that sedimentary eDNA could preserve the ecological structure of the entire pelagic community, including non-fossilized taxa, thus opening new avenues for paleoceanographic and paleoecological studies.Publisher PDFPeer reviewe

Metabarcoding analysis on European coastal samples reveals new molecular metazoan diversity

Although animals are among the best studied organisms, we still lack a full description of their diversity, especially for microscopic taxa. This is partly due to the time-consuming and costly nature of surveying animal diversity through morphological and molecular studies of individual taxa. A powerful alternative is the use of high-throughput environmental sequencing, providing molecular data from all organisms sampled. We here address the unknown diversity of animal phyla in marine environments using an extensive dataset designed to assess eukaryotic ribosomal diversity among European coastal locations. A multi-phylum assessment of marine animal diversity that includes water column and sediments, oxic and anoxic environments, and both DNA and RNA templates, revealed a high percentage of novel 18S rRNA sequences in most phyla, suggesting that marine environments have not yet been fully sampled at a molecular level. This novelty is especially high among Platyhelminthes, Acoelomorpha, and Nematoda, which are well studied from a morphological perspective and abundant in benthic environments. We also identified, based on molecular data, a potentially novel group of widespread tunicates. Moreover, we recovered a high number of reads for Ctenophora and Cnidaria in the smaller fractions suggesting their gametes might play a greater ecological role than previously suspected

Enhanced monitoring of life in the sea is a critical component of conservation management and sustainable economic growth

Marine biodiversity is a fundamental characteristic of our planet that depends on and influences climate, water quality, and many ocean state variables. It is also at the core of ecosystem services that can make or break economic development in any region. Our purpose is to highlight the need for marine biological observations to inform science and conservation management and to support the blue economy. We provide ten recommendations, applicable now, to measure and forecast biological Essential Ocean Variables (EOVs) as part of economic monitoring efforts. The UN Decade of Ocean Science for Sustainable Development (2021–2030) provides a timely opportunity to implement these recommendations to benefit humanity and enable the USD 3 trillion global ocean economy expected by 2030

A New Integrated Approach to Taxonomy: The Fusion of Molecular and Morphological Systematics with Type Material in Benthic Foraminifera

This work was supported by NERC grant NE4/G018502/1 and NE/G020310/1 (Website: http://www.nerc.ac.uk). The authors also thank the following for their support the Carnegie Trust for the Universities of Scotland (Website: http://www.carnegie-trust.org) and the Estuarine Coastal and Shelf Science Association (Website: http://www.ecsanews.org). M.S. was also supported by the Swiss National Science Foundation (SNSF), fellowships for advanced researchers PA00P2_126226 and PA00P2_142065 (Website: http://www.snf.ch/en/Pages/default.aspx).A robust and consistent taxonomy underpins the use of fossil material in palaeoenvironmental research and long-term assessment of biodiversity. This study presents a new integrated taxonomic protocol for benthic foraminifera by unequivocally reconciling the traditional taxonomic name to a specific genetic type. To implement this protocol, a fragment of the small subunit ribosomal RNA (SSU rRNA) gene is used in combination with 16 quantitative morphometric variables to fully characterise the benthic foraminiferal species concept of Elphidium williamsoni Haynes, 1973. A combination of live contemporary topotypic specimens, original type specimens and specimens of genetic outliers were utilised in this study. Through a series of multivariate statistical tests we illustrate that genetically characterised topotype specimens are morphologically congruent with both the holotype and paratype specimens of E. williamsoni Haynes, 1973. We present the first clear link between morphologically characterised type material and the unique SSU rRNA genetic type of E. williamsoni. This example provides a standard framework for the benthic foraminifera which bridges the current discontinuity between molecular and morphological lines of evidence, allowing integration with the traditional Linnaean roots of nomenclature to offer a new prospect for taxonomic stability.Publisher PDFPeer reviewe

Ancient DNA sheds new light on the Svalbard foraminiferal fossil record of the last millennium

International audienceRecent palaeogenetic studies have demonstrated the occurrence of preserved ancient DNA (aDNA) in various types of fossilised material. Environmental aDNA sequences assigned to modern species have been recovered from marine sediments dating to the Pleistocene. However, the match between the aDNA and the fossil record still needs to be evaluated for the environmental DNA approaches to be fully exploited. Here, we focus on foraminifera in sediments up to one thousand years old retrieved from the Hornsund fjord (Svalbard). We compared the diversity of foraminiferal microfossil assemblages with the diversity of aDNA sequenced from subsurface sediment samples using both cloning and high-throughput sequencing (HTS). Our study shows that 57% of the species archived in the fossil record were also detected in the aDNA data. However, the relative abundance of aDNA sequence reads and fossil specimens differed considerably. We also found a limited match between the stratigraphic occurrence of some fossil species and their aDNA sequences, especially in the case of rare taxa. The aDNA data comprised a high proportion of non-fossilised monothalamous species, which are known to dominate in modern foraminiferal communities of the Svalbard region. Our results confirm the relevance of HTS for studying past micro-eukaryotic diversity and provide insight into its ability to reflect fossil assemblages. Palaeogenetic studies including aDNA analyses of non-fossilised groups expand the range of palaeoceanographical proxies and therefore may increase the accuracy of palaeoenvironmental reconstructions

Environmental RNA outperforms eDNA metabarcoding in assessing impact of marine pollution: A chromium-spiked mesocosm test

Environmental (e)DNA metabarcoding holds great promise for biomonitoring and ecotoxicological applications. However, few studies have compared the performance of eDNA versus eRNA metabarcoding in assessing organismal response to marine pollution, in experimental conditions. Here, we performed a chromium (Cr)-spiked mesocosm experimental test on benthic foraminiferal community to investigate the effects on species diversity by analysing both eDNA and eRNA metabarcoding data across different Cr concentrations in the sediment. Foraminiferal diversity in the eRNA data showed a significant negative correlation with the Cr concentration in the sediment, while a positive response was observed in the eDNA data. The foraminiferal OTUs exhibited a higher turnover rate in eRNA than in the eDNA-derived community. Furthermore, in the eRNA samples, OTUs abundance was significantly affected by the Cr gradient in the sediment (Pseudo-R2 = 0.28, p = 0.05), while no significant trend was observed in the eDNA samples. The correlation between Cr concentration and foraminiferal diversity in eRNA datasets was stronger when the less abundant OTUs (&lt;100 reads) were removed and the analyses were conducted exclusively on OTUs shared between eRNA and eDNA datasets. This indicates the importance of metabarcoding data filtering to capture ecological impacts, in addition to using the putatively active organisms in the eRNA dataset. The comparative analyses on foraminiferal diversity revealed that eRNA-based metabarcoding can better assess the response to heavy metal exposure in presence of subtle concentrations of the pollutant. Furthermore, our results suggest that to unlock the full potential for ecosystem assessment, eDNA and eRNA should be studied in parallel to control for potential sequence artifacts in routine ecosystem surveys