Uncovering potential mangrove microbial bioindicators to assess urban and agricultural pressures on Martinique island in the eastern Caribbean Sea.

Martinique's mangroves, which cover 1.85 ha of the island (<0.1 % of the total area), are considerably vulnerable to local urban, agricultural, and industrial pollutants. Unlike for temperate ecosystems, there are limited indicators that can be used to assess the anthropogenic pressures on mangroves. This study investigated four stations on Martinique Island, with each being subject to varying anthropogenic pressures. An analysis of mangrove sediment cores approximately 18 cm in depth revealed two primary types of pressures on Martinique mangroves: (i) an enrichment in organic matter in the two stations within the highly urbanized bay of Fort-de-France and (ii) agricultural pressure observed in the four studied mangrove stations. This pressure was characterized by contamination, exceeding the regulatory thresholds, with dieldrin, total DDT, and metals (As, Cu and Ni) found in phytosanitary products. The mangroves of Martinique are subjected to varying degrees of anthropogenic pressure, but all are subjected to contamination by organochlorine pesticides. Mangroves within the bay of Fort-de-France experience notably higher pressures compared to those in the island's northern and southern regions. In these contexts, the microbial communities exhibited distinct responses. The microbial biomass and the abundance of bacteria and archaea were higher in the two less-impacted stations, while in the mangrove of Fort-de-France, various phyla typically associated with polluted environments were more prevalent. These differences in the microbiota composition led to the identification of 65 taxa, including Acanthopleuribacteraceae, Spirochaetaceae, and Pirellulaceae, that could potentially serve as indicators of an anthropogenic influence on the mangrove sediments of Martinique Island.

Are clam-seagrass interactions affected by heatwaves during emersion?

The increased frequency of heatwaves expected in the context of global warming will affect socio-ecological systems such as shellfish beds at intertidal seagrass meadows. A mesocosm experiment was performed to assess the effects of a simulated atmospheric heatwave during low tide on the bioturbation indicators and growth of the commercial juvenile native Ruditapes decussatus and the introduced clam R. philippinarum, and on their interactions with the seagrass Zostera noltei. Under the heatwave, heat dissipation at 5 cm depth was significantly greater in the sediments below Z. noltei than below bare sand, the photosynthetic efficiency (Fv/Fm) of Z. noltei decreased and the clams tended to grow less. Furthermore, after the heatwave clams below bare sand tended to burrow deeper than those below Z. noltei, indicating that seagrass provided a refuge for clams. Ruditapes philippinarum grew less, and did not burrow as deeply as R. decussatus, which may imply greater vulnerability to desiccation and heat at low tide. The particle displacement coefficient (PDC) of R. philippinarum indicated lower bioturbation values in Z. noltei than in bare sand and was a suitable bioturbation indicator for juvenile Ruditapes spp. clams. In Z. noltei coexisting with R. philippinarum, the Fv/Fm values were higher than without clams after a recovery period, which may be linked to the assimilation of phosphate excreted by the clams and suggests a facilitative interaction. No such interaction was observed with R. deccusatus, probably because of its deeper burrowing depth. The findings suggest reciprocal facilitative interactions between R. philippinarum and Z. noltei and the potential contribution of Z. noltei to the sustainability of clams under global warming scenarios, which may support management actions aimed at enhancing the coexistence between shellfishing activities and seagrass conservation.

Mangrove microbiota along the urban-to-rural gradient of the Cayenne estuary (French Guiana, South America): Drivers and potential bioindicators.

The microbial communities inhabiting the Atlantic-East Pacific (AEP) mangroves have been poorly studied, and mostly comprise chronically polluted mangroves. In this study, we characterized changes in the structure and diversity of microbial communities of mangroves along the urban-to-rural gradient of the Cayenne estuary (French Guiana, South America) that experience low human impact. The microbial communities were assigned into 50 phyla. Proteobacteria, Chloroflexi, Acidobacteria, Bacteroidetes, and Planctomycetes were the most abundant taxa. The environmental determinants found to significantly correlated to the microbial communities at these mangroves were granulometry, dieldrin concentration, pH, and total carbon (TC) content. Furthermore, a precise analysis of the sediment highlights the existence of three types of anthropogenic pressure among the stations: (i) organic matter (OM) enrichment due to the proximity to the city and its wastewater treatment plant, (ii) dieldrin contamination, and (iii) naphthalene contamination. These forms of weak anthropogenic pressure seemed to impact the bacterial population size and microbial assemblages. A decrease in Bathyarchaeota, "Candidatus Nitrosopumilus", and Nitrospira genera was observed in mangroves subjected to OM enrichment. Mangroves polluted with organic contaminants were enriched in Desulfobacteraceae, Desulfarculaceae, and Acanthopleuribacteraceae (with dieldrin or polychlorobiphenyl contamination), and Chitinophagaceae and Geobacteraceae (with naphthalene contamination). These findings provide insights into the main environmental factors shaping microbial communities of mangroves in the AEP that experience low human impact and allow for the identification of several potential microbial bioindicators of weak anthropogenic pressure.

Bioturbation effects on bioaccumulation of cadmium in the wetland plant Typha latifolia: A nature-based experiment.

The development of efficient bioremediation techniques to reduce aquatic pollutant load in natural sediment is one of the current challenges in ecological engineering. A nature-based solution for metal bioremediation is proposed through a combination of bioturbation and phytoremediation processes in experimental indoor microcosms. The invertebrates Tubifex tubifex (Oligochaeta Tubificidae) was used as an active ecological engineer for bioturbation enhancement. The riparian plant species Typha latifolia was selected for its efficiency in phyto-accumulating pollutants from sediment. Phytoremediation efficiency was estimated by using cadmium as a conservative pollutant known to bio-accumulate in plants, and initially introduced in the overlying water (20µg Cd/L of cadmium nitrate - Cd(NO3)2·4H2O). Biological sediment reworking by invertebrates' activity was quantified using luminophores (inert particulates). Our results showed that bioturbation caused by tubificid worms' activity followed the bio-conveying transport model with a downward vertical velocity (V) of luminophores ranging from 16.7±4.5 to 18.5±3.9cm·year-1. The biotransport changed the granulometric properties of the surface sediments, and this natural process was still efficient under cadmium contamination. The highest value of Cd enrichment coefficient for plant roots was observed in subsurface sediment layer (below 1cm to 5cm depth) with tubificids addition. We demonstrated that biotransport changed the distribution of cadmium across the sediment column as well as it enhanced the pumping of this metal from the surface to the anoxic sediment layers, thereby increasing the bioaccumulation of cadmium in the root system of Typha latifolia. This therefore highlights the potential of bioturbation as a tool to be considered in future as integrated bioremediation strategies of metallic polluted sediment in aquatic ecosystems.

Multistress effects on goldfish (Carassius auratus) behavior and metabolism.

Crossed effects between climate change and chemical pollutions were identified on community structure and ecosystem functioning. Temperature rising affects the toxic properties of pollutants and the sensitiveness of organisms to chemicals stress. Inversely, chemical exposure may decrease the capacity of organisms to respond to environmental changes. The aim of our study was to assess the individual and crossed effects of temperature rising and pesticide contamination on fish. Goldfish, Carassius auratus, were exposed during 96 h at two temperatures (22 and 32 °C) to a mixture of common pesticides (S-metolachlor, isoproturon, linuron, atrazine-desethyl, aclonifen, pendimethalin, and tebuconazol) at two environmentally relevant concentrations (total concentrations MIX1 = 8.4 µg L(-1) and MIX2 = 42 µg L(-1)). We investigated the sediment reworking behavior, which has a major ecological functional role. We also focused on three physiological traits from the cellular up to the whole individual level showing metabolic status of fish (protein concentration in liver and muscle, hepatosomatic index, and Fulton's condition factor). Individual thermal stress and low concentrations of pesticides decreased the sediment reworking activity of fish and entrained metabolic compensation with global depletion in energy stores. We found that combined chemical and thermal stresses impaired the capacity of fish to set up an efficient adaptive response. Our results strongly suggest that temperature will make fish more sensitive to water contamination by pesticides, raising concerns about wild fish conservation submitted to global changes.

Use of dispersant in mudflat oil-contaminated sediment: behavior and effects of dispersed oil on micro- and macrobenthos.

The present study aimed to examine whether the use of dispersant would be suitable for favoring the hydrocarbon degradation in coastal marine sediments without impacting negatively micro- and macrobenthic organisms. Mudflat sediments, maintained during 286 days in mesocosms designed to simulate natural conditions, were contaminated or not with Ural blend crude oil (REBCO) and treated or not with third-generation dispersant (Finasol OSR52). While the dispersant did not lead to an increase of hydrocarbon biodegradation, its use enables an attenuation of more than 55 % of the sediment concentration of total petroleum hydrocarbons (TPH). Canonical correspondence analysis (CCA) correlating T-RFLP patterns with the hydrocarbon content and bacterial abundance indicated weak differences between the different treatments except for the mesocosm treated with oil and dispersant for which a higher bacterial biomass was observed. The use of the dispersant did not significantly decrease the macrobenthic species richness or macroorganisms' densities in uncontaminated or contaminated conditions. However, even if the structure of the macrobenthic communities was not affected, when used in combination with oil, biological sediment reworking coefficient was negatively impacted. Although the use of the dispersant may be worth considering in order to accelerate the attenuation of hydrocarbon-contaminated mudflat sediments, long-term effects on functional aspects of the benthic system such as bioturbation and bacterial activity should be carefully studied before.

Dynamics of bacterial assemblages and removal of polycyclic aromatic hydrocarbons in oil-contaminated coastal marine sediments subjected to contrasted oxygen regimes.

To study the impact of oxygen regimes on the removal of polycylic aromatic hydrocarbons (PAHs) in oil-spill-affected coastal marine sediments, we used a thin-layer incubation method to ensure that the incubated sediment was fully oxic, anoxic, or was influenced by oxic-anoxic switches without sediment stirring. Hydrocarbon content and microbial assemblages were followed during 60 days to determine PAH degradation kinetics and microbial community dynamics according to the oxygenation regimes. The highest PAH removal, with 69 % reduction, was obtained at the end of the experiment under oxic conditions, whereas weaker removals were obtained under oscillating and anoxic conditions (18 and 12 %, respectively). Bacterial community structure during the experiment was determined using a dual 16S rRNA genes/16S rRNA transcripts approach, allowing the characterization of metabolically active bacteria responsible for the functioning of the bacterial community in the contaminated sediment. The shift of the metabolically active bacterial communities showed that the selection of first responders belonged to Pseudomonas spp. and Labrenzia sp. and included an unidentified Deltaproteobacteria-irrespective of the oxygen regime-followed by the selection of late responders adapted to the oxygen regime. A novel unaffiliated phylotype (B38) was highly active during the last stage of the experiment, at which time, the low-molecular-weight (LMW) PAH biodegradation rates were significant for permanent oxic- and oxygen-oscillating conditions, suggesting that this novel phylotype plays an active role during the restoration phase of the studied ecosystem.

Effect of physical sediments reworking on hydrocarbon degradation and bacterial community structure in marine coastal sediments.

The present study aimed to examine whether the physical reworking of sediments by harrowing would be suitable for favouring the hydrocarbon degradation in coastal marine sediments. Mudflat sediments were maintained in mesocosms under conditions as closer as possible to those prevailing in natural environments with tidal cycles. Sediments were contaminated with Ural blend crude oil, and in half of them, harrowing treatment was applied in order to mimic physical reworking of surface sediments. Hydrocarbon distribution within the sediment and its removal was followed during 286 days. The harrowing treatment allowed hydrocarbon compounds to penetrate the first 6 cm of the sediments, and biodegradation indexes (such as n-C18/phytane) indicated that biodegradation started 90 days before that observed in untreated control mesocosms. However, the harrowing treatment had a severe impact on benthic organisms reducing drastically the macrofaunal abundance and diversity. In the harrowing-treated mesocosms, the bacterial abundance, determined by 16S rRNA gene Q-PCR, was slightly increased; and terminal restriction fragment length polymorphism (T-RFLP) analyses of 16S rRNA genes showed distinct and specific bacterial community structure. Co-occurrence network and canonical correspondence analyses (CCA) based on T-RFLP data indicated the main correlations between bacterial operational taxonomic units (OTUs) as well as the associations between OTUs and hydrocarbon compound contents further supported by clustered correlation (ClusCor) analysis. The analyses highlighted the OTUs constituting the network structural bases involved in hydrocarbon degradation. Negative correlations indicated the possible shifts in bacterial communities that occurred during the ecological succession.

Oil spill effects on macrofaunal communities and bioturbation of pristine marine sediments (Caleta Valdés, Patagonia, Argentina): experimental evidence of low resistance capacities of benthic systems without history of pollution.

The Patagonian coast is characterized by the existence of pristine ecosystems which may be particularly sensitive to oil contamination. In this study, a simulated oil spill at acute and chronic input levels was carried out to assess the effects of contamination on the macrobenthic community structure and the bioturbation activity of sediments sampled in Caleta Valdés creek. Superficial sediments were either noncontaminated or contaminated by Escalante crude oil and incubated in the laboratory for 30 days. Oil contamination induced adverse effects on macrobenthic community at both concentrations with, for the highest concentration, a marked decrease of approximately 40 and 55 % of density and specific richness, respectively. Besides the disappearance of sensitive species, some other species like Oligochaeta sp. 1, Paranebalia sp., and Ostracoda sp. 2 species have a higher resistance to oil contamination. Sediment reworking activity was also affected by oil addition. At the highest level of contamination, nearly no activity was observed due to the high mortality of macroorganisms. The results strongly suggest that an oil spill in this protected marine area with no previous history of contamination would have a deep impact on the non-adapted macrobenthic community.

Functional response of an adapted subtidal macrobenthic community to an oil spill: macrobenthic structure and bioturbation activity over time throughout an 18-month field experiment.

An experimental oil spill was carried out in order to assess in situ responses of a macrobenthic community of shallow subtidal sediments historically exposed to petroleum contamination. Both structural and functional (bioturbation activity) parameters of the community, subjected or not to a pulse acute contamination (25,000 ppm), were studied for 18 months. No difference in the community structure was detected between contaminated and control sediments, from 6 to 18 months of experimentation. Vertical distributions of organisms, however, were affected by the presence of oil contamination leading to a deeper burial of some polychaete species. In the same time, changes in sediment-reworking activity and more especially a deeper particle burying in sediments subjected to acute oil contamination were shown. These results highlight the need to complete the analysis of community structure by assessing functional aspects, such as bioturbation activity, a process integrating various aspects of benthic behaviour (e.g. feeding, locomotion, burrow building) in order to estimate real (structural and functional) and long-term effects of oil contamination on benthic communities.

Impact of oil on bacterial community structure in bioturbated sediments.

Oil spills threaten coastlines where biological processes supply essential ecosystem services. Therefore, it is crucial to understand how oil influences the microbial communities in sediments that play key roles in ecosystem functioning. Ecosystems such as sediments are characterized by intensive bioturbation due to burrowing macrofauna that may modify the microbial metabolisms. It is thus essential to consider the bioturbation when determining the impact of oil on microbial communities. In this study, an experimental laboratory device maintaining pristine collected mudflat sediments in microcosms closer to true environmental conditions--with tidal cycles and natural seawater--was used to simulate an oil spill under bioturbation conditions. Different conditions were applied to the microcosms including an addition of: standardized oil (Blend Arabian Light crude oil, 25.6 mg.g⁻¹ wet sediment), the common burrowing organism Hediste (Nereis) diversicolor and both the oil and H. diversicolor. The addition of H. diversicolor and its associated bioturbation did not affect the removal of petroleum hydrocarbons. After 270 days, 60% of hydrocarbons had been removed in all microcosms irrespective of the H. diversicolor addition. However, 16S-rRNA gene and 16S-cDNA T-RFLP and RT-PCR-amplicon libraries analysis showed an effect of the condition on the bacterial community structure, composition, and dynamics, supported by PerMANOVA analysis. The 16S-cDNA libraries from microcosms where H. diversicolor was added (oiled and un-oiled) showed a marked dominance of sequences related to Gammaproteobacteria. However, in the oiled-library sequences associated to Deltaproteobacteria and Bacteroidetes were also highly represented. The 16S-cDNA libraries from oiled-microcosms (with and without H. diversicolor addition) revealed two distinct microbial communities characterized by different phylotypes associated to known hydrocarbonoclastic bacteria and dominated by Gammaproteobacteria and Deltaproteobacteria. In the oiled-microcosms, the addition of H. diversicolor reduced the phylotype-richness, sequences associated to Actinobacteria, Firmicutes and Plantomycetes were not detected. These observations highlight the influence of the bioturbation on the bacterial community structure without affecting the biodegradation capacities.

Characterization of specificity of bacterial community structure within the burrow environment of the marine polychaete Hediste (Nereis) diversicolor.

Bioturbation is known to stimulate microbial communities, especially in macrofaunal burrows where the abundance and activities of bacteria are increased. Until now, these microbial communities have been poorly characterized and an important ecological question remains: do burrow walls harbor similar or specific communities compared with anoxic and surface sediments? The bacterial community structure of coastal sediments inhabited by the polychaete worm Hediste diversicolor was investigated. Surface, burrow wall and anoxic sediments were collected at the Carteau beach (Gulf of Fos, Mediterranean Sea). Bacterial diversity was determined by analyzing small subunit ribosomal RNA (16S rRNA) sequences from three clone libraries (168, 179 and 129 sequences for the surface, burrow wall and anoxic sediments, respectively). Libraries revealed 306 different operational taxonomic units (OTUs) belonging to at least 15 bacterial phyla. Bioinformatic analyses and comparisons between the three clone libraries showed that the burrow walls harbored a specific bacterial community structure which differed from the surface and anoxic environments. More similarities were nevertheless found with the surface assemblage. Inside the burrow walls, the bacterial community was characterized by high biodiversity, which probably results from the biogeochemical heterogeneity of the burrow system.

Influence of bioturbation by the polychaete Nereis diversicolor on the structure of bacterial communities in oil contaminated coastal sediments.

Patterns of change in the structure of bacterial communities monitored by ribosomal intergenic spacer analysis (RISA) in oil contaminated sediments inhabited or not by the marine polychaete Nereis diversicolor were studied during 45 days under laboratory conditions. Results supported by principal component analysis showed a marked response of the bacterial communities to the oil contamination and to the presence of N. diversicolor. Phylogenetic affiliation of specific RISA bands showed that, in the contaminated sediments, the presence of the marine polychaetes favoured the development of bacteria which may play an active role in natural bioremediation processes of oil polluted environments.