High microbiome and metabolome diversification in coexisting sponges with different bio-ecological traits.

Marine Porifera host diverse microbial communities, which influence host metabolism and fitness. However, functional relationships between sponge microbiomes and metabolic signatures are poorly understood. We integrate microbiome characterization, metabolomics and microbial predicted functions of four coexisting Mediterranean sponges -Petrosia ficiformis, Chondrosia reniformis, Crambe crambe and Chondrilla nucula. Microscopy observations reveal anatomical differences in microbial densities. Microbiomes exhibit strong species-specific trends. C. crambe shares many rare amplicon sequence variants (ASV) with the surrounding seawater. This suggests important inputs of microbial diversity acquired by selective horizontal acquisition. Phylum Cyanobacteria is mainly represented in C. nucula and C. crambe. According to putative functions, the microbiome of P. ficiformis and C. reniformis are functionally heterotrophic, while C. crambe and C. nucula are autotrophic. The four species display distinct metabolic profiles at single compound level. However, at molecular class level they share a "core metabolome". Concurrently, we find global microbiome-metabolome association when considering all four sponge species. Within each species still, sets of microbe/metabolites are identified driving multi-omics congruence. Our findings suggest that diverse microbial players and metabolic profiles may promote niche diversification, but also, analogous phenotypic patterns of "symbiont evolutionary convergence" in sponge assemblages where holobionts co-exist in the same area.

Fungal Abundance and Diversity in the Mariana Trench, the Deepest Ecosystem on Earth.

Hadal trenches host abundant and diversified benthic prokaryotic assemblages, but information on benthic fungi is still extremely limited. We investigated the fungal abundance and diversity in the Challenger Deep (at ca. 11,000 m depth) and the slope of the Mariana Trench in comparison with three sites of the adjacent abyssal plain. Our results indicate that trench sediments are a hotspot of fungal abundance in terms of the 18S rRNA gene copy number. The fungal diversity (as the number of amplicon sequence variants, ASVs) was relatively low at all sites (10-31 ASVs) but showed a high turnover diversity among stations due to the presence of exclusive fungal taxa belonging to Aspergillaceae, Trichosphaeriaceae, and Nectriaceae. Fungal abundance and diversity were closely linked to sediment organic matter content and composition (i.e., phytopigments and carbohydrates), suggesting a specialization of different fungal taxa for the exploitation of available resources. Overall, these findings provide new insights into the diversity of deep-sea fungi and the potential ecological role in trench sediments and pave the way for a better understanding of their relevance in one of the most extreme ecosystems on Earth.

Effects of seagrass (Cymodocea nodosa) restoration on nematode biodiversity.

Seagrass meadows are hot spots of biodiversity and play a key role in the provisioning of ecosystem goods and services but are often subjected to a regression due to a combination of multiple anthropogenic and climate-induced impacts. The ecological restoration of these habitat-forming species is a priority to reverse biodiversity loss and for the recovery of key ecosystem functions. Here we investigated the effects of seagrass (Cymodocea nodosa) restoration action on benthic biodiversity recovery assessed by a time-series analysis carried out for one year. We used nematode assemblages, the most widespread metazoan on global sediments, as a proxy of benthic biodiversity and compared the species richness, expected species number (ES51) and composition in donor and in restored seagrasses and in the adjacent unvegetated sediments. One year after the intervention, nematode biodiversity in restored seagrasses was more similar to that of the donor site than in unvegetated sediments, suggesting a progressive recovery. Overall, the nematode biodiversity of the restored seagrasses resulted in an intermediate level between unvegetated and pristine seagrass meadows, providing evidence that restoration intervention contributed to biodiversity recovery. Pristine and restored seagrass meadows hosted a high number of exclusive species, which resulted in an increase in the overall biodiversity in the investigated location. Our results indicate that the restoration of seagrass meadows has positive effects on benthic biodiversity and contributes to enhance the local biodiversity.

Viral Diversity in Benthic Abyssal Ecosystems: Ecological and Methodological Considerations.

Viruses are the most abundant 'biological entities' in the world's oceans. However, technical and methodological constraints limit our understanding of their diversity, particularly in benthic abyssal ecosystems (>4000 m depth). To verify advantages and limitations of analyzing virome DNA subjected either to random amplification or unamplified, we applied shotgun sequencing-by-synthesis to two sample pairs obtained from benthic abyssal sites located in the North-eastern Atlantic Ocean at ca. 4700 m depth. One amplified DNA sample was also subjected to single-molecule long-read sequencing for comparative purposes. Overall, we identified 24,828 viral Operational Taxonomic Units (vOTUs), belonging to 22 viral families. Viral reads were more abundant in the amplified DNA samples (38.5-49.9%) compared to the unamplified ones (4.4-5.8%), with the latter showing a greater viral diversity and 11-16% of dsDNA viruses almost undetectable in the amplified samples. From a procedural point of view, the viromes obtained by direct sequencing (without amplification step) provided a broader overview of both ss and dsDNA viral diversity. Nevertheless, our results suggest that the contextual use of random amplification of the same sample and long-read technology can improve the assessment of viral assemblages by reducing off-target reads.

Bioaccumulation and biomagnification of heavy metals in marine micro-predators.

Nematodes represent >3/5 of the abundance of the world's metazoans and usually account for nearly 90% of the total benthic fauna, playing a key ecological role in the benthic ecosystem functioning on a global scale. These small metazoans include a relevant number of microscopic predators and, in turn, are the most abundant preys of macro-megafauna and fish juveniles thus playing a key role in marine food webs. Here, using two independent approaches, we test the bioaccumulation in marine nematodes of several heavy metals present in contaminated sediments. We report here that nematodes, despite their short life cycle and small size, bioaccumulate significantly heavy metals. Bioaccumulation increases from deposit feeders and microalgal grazers to predators of microbes and other tiny metazoans. These results suggest that nematodes also contribute to their biomagnification along the food webs and can contribute to increase the transfer of contaminants from the sediments to larger organisms.

Rhodobacteraceae dominate the core microbiome of the sea star Odontaster validus (Koehler, 1906) in two opposite geographical sectors of the Antarctic Ocean.

Microbiota plays essential roles in the health, physiology, and in adaptation of marine multi-cellular organisms to their environment. In Antarctica, marine organisms have a wide range of unique physiological functions and adaptive strategies, useful for coping with extremely cold conditions. However, the role of microbiota associated with Antarctic organisms in such adaptive strategies is underexplored. In the present study, we investigated the diversity and putative functions of the microbiome of the sea star Odontaster validus, one of the main keystone species of the Antarctic benthic ecosystems. We compared the whole-body bacterial microbiome of sea stars from different sites of the Antarctic Peninsula and Ross Sea, two areas located in two opposite geographical sectors of the Antarctic continent. The taxonomic composition of O. validus microbiomes changed both between and within the two Antarctic sectors, suggesting that environmental and biological factors acting both at large and local scales may influence microbiome diversity. Despite this, one bacterial family (Rhodobacteraceae) was shared among all sea star individuals from the two geographical sectors, representing up to 95% of the microbial core, and suggesting a key functional role of this taxon in holobiont metabolism and well-being. In addition, the genus Roseobacter belonging to this family was also present in the surrounding sediment, implying a potential horizontal acquisition of dominant bacterial core taxa via host-selection processes from the environment.

Encapsulated in sediments: eDNA deciphers the ecosystem history of one of the most polluted European marine sites.

The Anthropocene is characterized by dramatic ecosystem changes driven by human activities. The impact of these activities can be assessed by different geochemical and paleontological proxies. However, each of these proxies provides only a fragmentary insight into the effects of anthropogenic impacts. It is highly challenging to reconstruct, with a holistic view, the state of the ecosystems from the preindustrial period to the present day, covering all biological components, from prokaryotes to multicellular eukaryotes. Here, we used sedimentary ancient DNA (sedaDNA) archives encompassing all trophic levels of biodiversity to reconstruct the two century-natural history in Bagnoli-Coroglio (Gulf of Pozzuoli, Tyrrhenian Sea), one of the most polluted marine-coastal sites in Europe. The site was characterized by seagrass meadows and high eukaryotic diversity until the beginning of the 20th century. Then, the ecosystem completely changed, with seagrasses and associated fauna as well as diverse groups of planktonic and benthic protists being replaced by low diversity biota dominated by dinophyceans and infaunal metazoan species. The sedaDNA analysis revealed a five-phase evolution of the area, where changes appear as the result of a multi-level cascade effect of impacts associated with industrial activities, urbanization, water circulation and land-use changes. The sedaDNA allowed to infer reference conditions that must be considered when restoration actions are to be implemented.

Microbiome enrichment from contaminated marine sediments unveils novel bacterial strains for petroleum hydrocarbon and heavy metal bioremediation.

Petroleum hydrocarbons and heavy metals are some of the most widespread contaminants affecting marine ecosystems, urgently needing effective and sustainable remediation solutions. Microbial-based bioremediation is gaining increasing interest as an effective, economically and environmentally sustainable strategy. Here, we hypothesized that the heavily polluted coastal area facing the Sarno River mouth, which discharges >3 tons of polycyclic aromatic hydrocarbons (PAHs) and ∼15 tons of heavy metals (HMs) into the sea annually, hosts unique microbiomes including marine bacteria useful for PAHs and HMs bioremediation. We thus enriched the microbiome of marine sediments, contextually selecting for HM-resistant bacteria. The enriched mixed bacterial culture was subjected to whole-DNA sequencing, metagenome-assembled-genomes (MAGs) annotation, and further sub-culturing to obtain the major bacterial species as pure strains. We obtained two novel isolates corresponding to the two most abundant MAGs (Alcanivorax xenomutans strain-SRM1 and Halomonas alkaliantarctica strain-SRM2), and tested their ability to degrade PAHs and remove HMs. Both strains exhibited high PAHs degradation (60-100%) and HMs removal (21-100%) yield, and we described in detail >60 genes in their MAGs to unveil the possible genetic basis for such abilities. Most promising yields (∼100%) were obtained towards naphthalene, pyrene and lead. We propose these novel bacterial strains and related genetic repertoire to be further exploited for effective bioremediation of marine environments contaminated with both PAHs and HMs.

Microbiome network in the pelagic and benthic offshore systems of the northern Adriatic Sea (Mediterranean Sea).

Because of their recognized global importance, there is now the urgent need to map diversity and distribution patterns of marine microbial communities. Even if available studies provided some advances in the understanding the biogeographical patterns of marine microbiomes at the global scale, their degree of plasticity at the local scale it is still underexplored, and functional implications still need to be dissected. In this scenario here we provide a synoptical study on the microbiomes of the water column and surface sediments from 19 sites in a 130 km2 area located 13.5 km afar from the coast in the North-Western Adriatic Sea (Italy), providing the finest-scale mapping of marine microbiomes in the Mediterranean Sea. Pelagic and benthic microbiomes in the study area showed sector specific-patterns and distinct assemblage structures, corresponding to specific variations in the microbiome network structure. While maintaining a balanced structure in terms of potential ecosystem services (e.g., hydrocarbon degradation and nutrient cycling), sector-specific patterns of over-abundant modules-and taxa-were defined, with the South sector (the closest to the coast) characterized by microbial groups of terrestrial origins, both in the pelagic and the benthic realms. By the granular assessment of the marine microbiome changes at the local scale, we have been able to describe, to our knowledge at the first time, the integration of terrestrial microorganisms in the marine microbiome networks, as a possible natural process characterizing eutrophic coastal area. This raises the question about the biological threshold for terrestrial microorganisms to be admitted in the marine microbiome networks, without altering the ecological balance.

Fungi Can Be More Effective than Bacteria for the Bioremediation of Marine Sediments Highly Contaminated with Heavy Metals.

The contamination of coastal marine sediments with heavy metals (HMs) is a widespread phenomenon that requires effective remediation actions. Bioremediation based on the use of bacteria is an economically and environmentally sustainable effective strategy for reducing HM contamination and/or toxicity in marine sediments. However, information on the efficiency of marine-derived fungi for HM decontamination of marine sediments is still largely lacking, despite evidence of the performance of terrestrial fungal strains on other contaminated matrixes (e.g., soils, freshwater sediments, industrial wastes). Here, we carried out for the first time an array of parallel laboratory experiments by using different combinations of chemical and microbial amendments (including acidophilic autotrophic and heterotrophic bacteria, as well as filamentous marine fungi) for the bioremediation of highly HM-contaminated sediments of the Portman Bay (NW Mediterranean Sea), an area largely affected by long-term historical discharges of mine tailings. Our results indicate that the bioleaching performance of metals from the sediment is based on the addition of fungi (Aspergillus niger and Trichoderma sp.), either alone or in combination with autotrophic bacteria, was higher when compared to other treatments. In particular, fungal addition allowed obtaining bioleaching yields for As eight times higher than those by chemical treatments and double compared with the addition of bacteria alone. Moreover, in our study, the fungal addition was the only treatment allowing effective bioleaching of otherwise not mobile fractions of Zn and Cd, thus overtaking bacterial treatments. We found that the lower the sediment pH reached by the experimental conditions, as in the case of fungal addition, the higher the solubilization yield of metals, suggesting that the specific metabolic features of A. niger and Trichoderma sp. enable lowering sediment pH and enhance HM bioleaching. Overall, our findings indicate that fungi can be more effective than acidophilic autotrophic and heterotrophic bacteria in HM bioleaching, and as such, their use can represent a promising and efficient strategy for the bioremediation of marine sediments highly contaminated with heavy metals.

Impact of resuspended mine tailings on benthic biodiversity and ecosystem processes: The case study of Portmán Bay, Western Mediterranean Sea, Spain.

Industrial seabed mining is expected to cause significant impacts on marine ecosystems, including physical disturbance and the generation of plumes of toxin-laden water. Portmán Bay (NW Mediterranean Sea), where an estimated amount of 60 Mt of mine tailings from sulphide ores were dumped from 1957 to 1990, is one of the most metal-polluted marine areas in Europe and worldwide. This bay can be used to assess the impact on marine ecosystems of particle settling from sediment plumes resulting from mine tailings resuspension. With this purpose in mind, we conducted a field experiment there to investigate subsequent effects of deposition of (artificially resuspended) contaminated sediments on (i) prokaryotic abundance and meiofaunal assemblages (in terms of abundance and diversity), (ii) the availability of trophic resources (in terms of organic matter biochemical composition), and (iii) a set of ecosystem functions including meiofaunal biomass, heterotrophic C production and C degradation rates. The results of this study show that mine tailings resuspension and plume deposition led to the decline of prokaryotic abundance and nematode's biodiversity. The later decreased because of species removal and transfer along with particle resuspension and plume deposition. Such changes were also associated to a decrease of the proteins content in the sediment organic matter, faster C degradation rates and higher prokaryotic C production. Overall, this study highlights that mine tailing resuspension and ensuing particle deposition can have deleterious effects on both prokaryotes and nematode diversity, alter biogeochemical cycles and accelerate C degradation rates. These results should be considered for the assessment of the potential effects of seabed mineral exploitation on marine ecosystems at large.

Changes in coral forest microbiomes predict the impact of marine heatwaves on habitat-forming species down to mesophotic depths.

Global warming is causing the increase in intensity and frequency of heatwaves, which are often associated with mass mortality events of marine organisms from shallow and mesophotic rocky habitats, including gorgonians and other sessile organisms. We investigated the microbiome responses of the gorgonians Paramuricea clavata, Eunicella cavolini, and the red coral Corallium rubrum to the episodic temperature anomalies detected in the North Western Mediterranean, during August 2011. Although the investigated corals showed no signs of visible necrosis, the abundance of associated Bacteria and Archaea increased with increasing seawater temperature, suggesting their temperature-dependent proliferation. Coral microbiomes were highly sensitive to thermal anomaly amplitude and exhibited increased bacterial diversity to greater thermal shifts. This effect was explained by the decline of dominant bacterial members and the increase of new, rare and opportunistic taxa, including pathogens, revealing a direct effect of heatwave-induced alteration of the microbiomes and not a secondary consequence of coral necrosis.

Local Environmental Conditions Promote High Turnover Diversity of Benthic Deep-Sea Fungi in the Ross Sea (Antarctica).

Fungi are a ubiquitous component of marine systems, but their quantitative relevance, biodiversity and ecological role in benthic deep-sea ecosystems remain largely unexplored. In this study, we investigated fungal abundance, diversity and assemblage composition in two benthic deep-sea sites of the Ross Sea (Southern Ocean, Antarctica), characterized by different environmental conditions (i.e., temperature, salinity, trophic availability). Our results indicate that fungal abundance (estimated as the number of 18S rDNA copies g-1) varied by almost one order of magnitude between the two benthic sites, consistently with changes in sediment characteristics and trophic availability. The highest fungal richness (in terms of Amplicon Sequence Variants-ASVs) was encountered in the sediments characterized by the highest organic matter content, indicating potential control of trophic availability on fungal diversity. The composition of fungal assemblages was highly diverse between sites and within each site (similarity less than 10%), suggesting that differences in environmental and ecological characteristics occurring even at a small spatial scale can promote high turnover diversity. Overall, this study provides new insights on the factors influencing the abundance and diversity of benthic deep-sea fungi inhabiting the Ross Sea, and also paves the way for a better understanding of the potential responses of benthic deep-sea fungi inhabiting Antarctic ecosystems in light of current and future climate changes.

Metagenome-assembled genome (MAG) of Oceancaulis alexandrii NP7 isolated from Mediterranean Sea polluted marine sediments and its bioremediation potential.

Oceanicaulis alexandrii strain NP7 is a marine bacterium which belongs to the Hyphomonadaceae family and was isolated from sediments highly contaminated with metals and polycyclic aromatic hydrocarbons released for decades by industrial activities in the Gulf of Naples (Mediterranean Sea). Here, we report the partial genome sequence and annotation of O. alexandrii strain NP7 that contains a chromosome of 2,954,327 bp and encodes for 2914 predicted coding sequences (CDSs) and 44 RNA-encoding genes. Although the presence of some CDSs for genes involved in hydrocarbon degradation processes (e.g., alkB) have already been described in the literature associated with the Oceanicaulis, this is the first time that more than 100 genes involved in metal detoxification processes and hydrocarbon degradation are reported belonging to this genus. The presence of a heterogeneous set of genes involved in stress response, hydrocarbon degradation, heavy metal resistance, and detoxification suggests a possible role for O. alexandrii NP7 in the bioremediation of these highly contaminated marine sediments.

Bacteria, Fungi and Microalgae for the Bioremediation of Marine Sediments Contaminated by Petroleum Hydrocarbons in the Omics Era.

Petroleum hydrocarbons (PHCs) are one of the most widespread and heterogeneous organic contaminants affecting marine ecosystems. The contamination of marine sediments or coastal areas by PHCs represents a major threat for the ecosystem and human health, calling for urgent, effective, and sustainable remediation solutions. Aside from some physical and chemical treatments that have been established over the years for marine sediment reclamation, bioremediation approaches based on the use of microorganisms are gaining increasing attention for their eco-compatibility, and lower costs. In this work, we review current knowledge concerning the bioremediation of PHCs in marine systems, presenting a synthesis of the most effective microbial taxa (i.e., bacteria, fungi, and microalgae) identified so far for hydrocarbon removal. We also discuss the challenges offered by innovative molecular approaches for the design of effective reclamation strategies based on these three microbial components of marine sediments contaminated by hydrocarbons.

Diversity, Ecological Role and Biotechnological Potential of Antarctic Marine Fungi.

The Antarctic Ocean is one of the most remote and inaccessible environments on our planet and hosts potentially high biodiversity, being largely unexplored and undescribed. Fungi have key functions and unique physiological and morphological adaptations even in extreme conditions, from shallow habitats to deep-sea sediments. Here, we summarized information on diversity, the ecological role, and biotechnological potential of marine fungi in the coldest biome on Earth. This review also discloses the importance of boosting research on Antarctic fungi as hidden treasures of biodiversity and bioactive molecules to better understand their role in marine ecosystem functioning and their applications in different biotechnological fields.

Highly Contaminated Marine Sediments Can Host Rare Bacterial Taxa Potentially Useful for Bioremediation.

Coastal areas impacted by high anthropogenic pressures typically display sediment contamination by polycyclic aromatic hydrocarbons (PAHs) and heavy metals (HMs). Microbial-based bioremediation represents a promising strategy for sediment reclamation, yet it frequently fails due to poor knowledge of the diversity and dynamics of the autochthonous microbial assemblages and to the inhibition of the target microbes in the contaminated matrix. In the present study, we used an integrated approach including a detailed environmental characterization, high-throughput sequencing and culturing to identify autochthonous bacteria with bioremediation potential in the sediments of Bagnoli-Coroglio (Gulf of Naples, Mediterranean Sea), a coastal area highly contaminated by PAHs, aliphatic hydrocarbons and HMs. The analysis of the benthic prokaryotic diversity showed that the distribution of the dominant taxon (Gammaproteobacteria) was mainly influenced by PAHs, As, and Cd concentrations. The other abundant taxa (including Alphaproteobacteria, Deltaproteobacteria, Bacteroidetes, Acidobacteria, Actinobacteria, NB1-j, Desulfobacterota, and Myxococcota) were mainly driven by sediment grain size and by Cu and Cr concentrations, while the rare taxa (i.e., each contributing <1%) by As and aliphatic hydrocarbons concentrations and by sediment redox potential. These results suggest a differential response of bacterial taxa to environmental features and chemical contamination and those different bacterial groups may be inhibited or promoted by different contaminants. This hypothesis was confirmed by culturing and isolating 80 bacterial strains using media highly enriched in PAHs, only nine of which were contextually resistant to high HM concentrations. Such resistant isolates represented novel Gammaproteobacteria strains affiliated to Vibrio, Pseudoalteromonas, and Agarivorans, which were only scarcely represented in their original assemblages. These findings suggest that rare but culturable bacterial strains resistant/tolerant to high levels of mixed contaminants can be promising candidates useful for the reclamation by bioaugmentation strategies of marine sediments that are highly contaminated with PAHs and HMs.

Genome Sequence of an Alkaliphilus Species Isolated from Historically Contaminated Sediments of the Gulf of Naples (Mediterranean Sea).

Here, we report the draft genome sequence of a metagenome-assembled genome (MAG) of a new Alkaliphilus bacterium, NP8, of the Clostridiaceae family. This bacterium was isolated from polluted sediment collected from an abandoned industrial site located in the Gulf of Naples (Mediterranean Sea) as part of a microbial consortium.

Multiple impacts of microplastics can threaten marine habitat-forming species.

Microplastics are recognised as a potential global threat to marine ecosystems, but the biological mechanisms determining their impact on marine life are still largely unknown. Here, we investigated the effects of microplastics on the red coral, a long-lived habitat-forming organism belonging to the Corallium genus, which is present at almost all latitudes from shallow-water to deep-sea habitats. When exposed to microplastics, corals preferentially ingest polypropylene, with multiple biological effects, from feeding impairment to mucus production and altered gene expression. Microplastics can alter the coral microbiome directly and indirectly by causing tissue abrasions that allow the proliferation of opportunistic bacteria. These multiple effects suggest that microplastics at the concentrations present in some marine areas and predicted for most oceans in the coming decades, can ultimately cause coral death. Other habitat-forming suspension-feeding species are likely subjected to similar impacts, which may act synergistically with climate-driven events primarily responsible for mass mortalities.

Sensitivity of foraminiferal-based indices to evaluate the ecological quality status of marine coastal benthic systems: A case study of the Gulf of Manfredonia (southern Adriatic Sea).

This paper aims to compare two foraminiferal based biotic indices generally used to evaluate the ecological quality status (EcoQS): the Foram-AMBI and the Foram Stress Index (FSI). For this purpose, we report the distribution and diversity of living foraminiferal assemblages and the environmental variables from a bathymetric transect in the Southern Adriatic Sea. The two indices agree well with the detected organic enrichment but indicate conflicting EcoQS as the Foram-AMBI detects good environmental conditions, whereas the FSI describes a poor-moderate quality. Many species not assigned (including soft-shelled foraminifera) are to blame for the different results. Also, both foraminiferal-based indices neglect the heavy metal increase encountered in the deepest stations. These findings suggest the need for a more in-depth analysis to improve the ecological status evaluation of marine benthic systems, including other descriptors as chemical pollutants in combination with biotic indices sensitive to organic matter enrichment.