Trace elements in the water column of high-altitude Pyrenean lakes: Impact of local weathering and long-range atmospheric input.

High altitude (alpine) lakes are efficient sentinels of environmental processes, including local pollution and long-range atmospheric transfer, because these lakes are highly vulnerable to ongoing climate changes and increasing anthropogenic pressure. Towards improving the knowledge of trace element geochemistry in the water column of alpine lakes, we assessed 64 physico-chemical parameters, including macro- and micronutrients, major and trace element concentrations in the water column of 18 lakes in the Pyrenees, located along the border between France and Spain. Lake depth, morphology, retention time and watershed rock lithology did not exhibit sizable impact on major and trace element concentrations in the water column. However, acidic (pH = 4.7 ± 0.2) lakes were distinctly different from circumneutral lakes (pH = 6.8 ± 0.5) as they exhibited >10 times higher concentrations of SO42- and trace metals (Fe, Mn, Zn, Cd, Pb, Co, Ni, Be, Al, Ga and REEs). While some of these elements clearly mark the presence of sulphide-rich minerals within the watershed (Fe, Zn, Cd and Pb), the increased mobility of lithogenic elements (Be, Al, Ga and REEs) in acidic lakes may reflect the leaching of these elements from silicate dust derived from atmospheric deposits or surrounding granites. At the same time, compared to circumneutral lakes, acidic lake water displayed lower concentrations of dissolved oxyanions (As, Mo, V, B and W) and elevated SO42- concentrations. The latter could lead to efficient Ba removal from the water column. The exploitation of metal ores within the watershed of three lakes clearly impacted high Zn and Cd concentrations observed in their water column, despite two of these lakes not being acidic. We conclude that local impacts have a greater effect on the water column than long-range atmospheric inputs and that dissolved trace element concentration measurements can be used for revealing sulphide-rich minerals or acid mine drainage within the lakes' watershed.

Distribution and genomic variation of ammonia-oxidizing archaea in abyssal and hadal surface sediments.

Ammonia-oxidizing archaea of the phylum Thaumarchaeota play a central role in the biogeochemical cycling of nitrogen in benthic sediments, at the interface between pelagic and subsurface ecosystems. However, our understanding of their niche separation and of the processes controlling their population structure in hadal and abyssal surface sediments is still limited. Here, we reconstructed 47 AOA metagenome-assembled genomes (MAGs) from surface sediments of the Atacama and Kermadec trench systems. They formed deep-sea-specific groups within the family Nitrosopumilaceae and were assigned to six amoA gene-based clades. MAGs from different clades had distinct distribution patterns along oxygen-ammonium counter gradients in surface sediments. At the species level, MAGs thus seemed to form different ecotypes and follow deterministic niche-based distributions. In contrast, intraspecific population structure, defined by patterns of Single Nucleotide Variants (SNV), seemed to reflect more complex contributions of both deterministic and stochastic processes. Firstly, the bathymetric range had a strong effect on population structure, with distinct populations in abyssal plains and hadal trenches. Then, hadal populations were clearly separated by trench system, suggesting a strong isolation-by-topography effect, whereas abyssal populations were rather controlled by sediment depth or geographic distances, depending on the clade considered. Interestingly, genetic variability between samples was lowest in sediment layers where the mean MAG coverage was highest, highlighting the importance of selective pressure linked with each AOA clade's ecological niche. Overall, our results show that deep-sea AOA genome distributions seem to follow both deterministic and stochastic processes, depending on the genomic variability scale considered.

Identifying macroplastic pathobiomes and antibiotic resistance in a subtropical fish farm.

Macroplastics are ubiquitous in aquaculture ecosystems. However, to date the potential role of plastics as a support for bacterial biofilm that can include potential human pathogenic bacteria (PHPB) and antibiotic-resistant bacteria (ARB) has been largely overlooked. In this study, we used a combination of metabarcoding and standard antibiotic susceptibility testing to study the pathobiome and resistome of macroplastics, fish guts and the environment in a marine aquaculture farm in Mauritius. Aquaculture macroplastics were found to be higher in PHPB, dominated by the Vibrionaceae family (0.34 % of the total community), compared with environmental samples. Moreover, isolates from aquaculture plastics showed higher significant multiple antibiotic resistance (MAR) compared to non-plastic samples of seawater, sediment and fish guts. These results suggest that plastics act as a reservoir and fomite of PHPB and ARB in aquaculture, potentially threatening the health of farmed fish and human consumers.

Metals and metalloids in high-altitude Pyrenean lakes: sources and distribution in pre-industrial and modern sediments.

High-altitude Pyrenean lakes are ecosystems far from local pollution sources, and thus they are particularly sensitive to the atmospheric deposition of metals and metalloids. This study aims to quantify the effect of human activity in 18 lakes located in both side of the France-Spain frontier. Sediment cores were collected in summer 2013, sampled at a 1cm resolution and the concentration of 24 elements was measured by ICP-MS. Statistic and chemometric analysis of the results highlights the influence of the geographical position and lithogenic features of each lake basin on trapping pollutants. More than the 80% of the lakes showed values of enrichment factor (EF) above 2 for at least one of the elements investigated in at least one core interval, which corroborates the existence of historical anthropogenic inputs of elements in the studied area. The results demonstrate the natural origin of As and Ti in Pyrenees, together with the significant anthropogenic inputs of Cd, Pb, Sb and Sn from ancient times. The data set points mining activities as the main historical source of pollution and illustrate the large impact of the industrial revolution. The regional variability could reflect also differential long-range transport, followed by dry or wet deposition.

Metagenomic data of bacterial communities associated with Acropora species from Phu Quoc Islands, Vietnam.

Acropora is one of the most common coral genera found in Phu Quoc Islands, Vietnam. However, the presence of marine snails, such as the coralllivorous gastropod Drupella rugosa, was a potential threat to the survival of many scleractinian species, leading to changes in the health status and bacterial diversity of coral reefs in Phu Quoc Islands. Here, we describe the composition of bacterial communities associated with two species of Acropora (Acropora formosa and Acropora millepora) using the Illumina sequencing technology. This dataset includes 5 coral samples of each status (grazed or healthy), which were collected in Phu Quoc Islands (9°55'20.6″N 104°01'16.4″E) in May 2020. A total of 19 phyla, 34 classes, 98 orders, 216 families and 364 bacterial genera were detected from 10 coral samples. Overall, Proteobacteria and Firmicutes were the two most common bacterial phyla in all samples. Significant differences in the relative abundances of the genera Fusibacter, Halarcobacter, Malaciobacter, and Thalassotalea between grazed and healthy status were observed. However, there was no differences in alpha diversity indices between the two status. Furthermore, the dataset analysis also indicated that Vibrio and Fusibacter were core genera in the grazed samples, whereas Pseudomonas was the core genus in the healthy samples.

Fishing for the Microbiome of Tropical Tuna.

Although tunas represent a significant part of the global fish economy and a major nutritional resource worldwide, their microbiome still remains poorly documented. Here, we conducted an analysis of the taxonomic composition of the bacterial communities inhabiting the gut, skin, and liver of two most consumed tropical tuna species (skipjack and yellowfin), from individuals caught in the Atlantic and Indian oceans. We hypothesized that each organ harbors a specific microbial assemblage whose composition might vary according to different biotic (sex, species) and/or abiotic (environmental) factors. Our results revealed that the composition of the tuna microbiome was totally independent of fish sex, regardless of the species and ocean considered. Instead, the main determinants of observed diversity were (i) tuna species for the gut and (ii) sampling site for the skin mucus layer and (iii) a combination of both parameters for the liver. Interestingly, 4.5% of all amplicon sequence variants (ASV) were shared by the three organs, highlighting the presence of a core-microbiota whose most abundant representatives belonged to the genera Mycoplasma, Cutibacterium, and Photobacterium. Our study also revealed the presence of a unique and diversified bacterial assemblage within the tuna liver, comprising a substantial proportion of potential histamine-producing bacteria, well known for their pathogenicity and their contribution to fish poisoning cases. These results indicate that this organ is an unexplored microbial niche whose role in the health of both the host and consumers remains to be elucidated.

Tracking spoilage bacteria in the tuna microbiome.

Like other seafood products, tuna is highly perishable and sensitive to microbial spoilage. Its consumption, whether fresh or canned, can lead to severe food poisoning due to the activity of specific microorganisms, including histamine-producing bacteria. Yet, many grey areas persist regarding their ecology, conditions of emergence, and proliferation in fish. In this study, we used 16S rRNA barcoding to investigate postmortem changes in the bacteriome of fresh and brine-frozen yellowfin tuna (Thunnus albacares), until late stages of decomposition (i.e. 120 h). The results revealed that despite standard refrigeration storage conditions (i.e. 4°C), a diverse and complex spoilage bacteriome developed in the gut and liver. The relative abundance of spoilage bacterial taxa increased rapidly in both organs, representing 82% of the bacterial communities in fresh yellowfin tuna, and less than 30% in brine-frozen tuna. Photobacterium was identified as one of the dominant bacterial genera, and its temporal dynamics were positively correlated with histamine concentration in both gut and liver samples, which ultimately exceeded the recommended sanitary threshold of 50 ppm in edible parts of tuna. The results from this study show that the sanitary risks associated with the consumption of this widely eaten fish are strongly influenced by postcapture storage conditions.

Shift and homogenization of gut microbiome during invasion in marine fishes.

Biological invasion is one of the main components of global changes in aquatic ecosystems. Unraveling how establishment in novel environments affects key biological features of animals is a key step towards understanding invasion. Gut microbiome of herbivorous animals is important for host health but has been scarcely assessed in invasive species. Here, we characterized the gut microbiome of two invasive marine herbivorous fishes (Siganus rivulatus and Siganus luridus) in their native (Red Sea) and invaded (Mediterranean Sea) ranges. The taxonomic and phylogenetic diversity of the microbiome increased as the fishes move away from the native range and its structure became increasingly different from the native microbiome. These shifts resulted in homogenization of the microbiome in the invaded range, within and between the two species. The shift in microbial diversity was associated with changes in its functions related with the metabolism of short-chain fatty acids. Altogether, our results suggest that the environmental conditions encountered by Siganidae during their expansion in Mediterranean ecosystems strongly modifies the composition of their gut microbiome along with its putative functions. Further studies should pursue to identify the precise determinants of these modifications (e.g. changes in host diet or behavior, genetic differentiation) and whether they participate in the ecological success of these species.

Diversity and Biogeography of Bathyal and Abyssal Seafloor Bacteria and Archaea Along a Mediterranean-Atlantic Gradient.

Seafloor sediments cover the majority of planet Earth and microorganisms inhabiting these environments play a central role in marine biogeochemical cycles. Yet, description of the biogeography and distribution of sedimentary microbial life is still too sparse to evaluate the relative contribution of processes driving this distribution, such as the levels of drift, connectivity, and specialization. To address this question, we analyzed 210 archaeal and bacterial metabarcoding libraries from a standardized and horizon-resolved collection of sediment samples from 18 stations along a longitudinal gradient from the eastern Mediterranean to the western Atlantic. Overall, we found that biogeographic patterns depended on the scale considered: while at local scale the selective influence of contemporary environmental conditions appeared strongest, the heritage of historic processes through dispersal limitation and drift became more apparent at regional scale, and ended up superseding contemporary influences at inter-regional scale. When looking at environmental factors, the structure of microbial communities was correlated primarily with water depth, with a clear transition between 800 and 1,200 meters below sea level. Oceanic basin, water temperature, and sediment depth were other important explanatory parameters of community structure. Finally, we propose increasing dispersal limitation and ecological drift with sediment depth as a probable factor for the enhanced divergence of deeper horizons communities.

Fishing for the Virome of Tropical Tuna.

While planktonic viruses have received much attention in recent decades, knowledge of the virome of marine organisms, especially fish, still remains rudimentary. This is notably the case with tuna, which are among the most consumed fish worldwide and represent considerable economic, social and nutritional value. Yet the composition of the tuna virome and its biological and environmental determinants remain unknown. To begin to address this gap, we investigated the taxonomic diversity of viral communities inhabiting the skin mucus, gut and liver of two major tropical tuna species (skipjack and yellowfin) in individuals fished in the Atlantic and Indian Oceans. While we found significant differences in the virome composition between the organs, this was totally independent of the tuna species or sex. The tuna virome was mainly dominated by eukaryotic viruses in the digestive organs (gut and liver), while bacteriophages were predominant in the mucus. We observed the presence of specific viral families in each organ, some previously identified as fish or human pathogens (e.g., Iridoviridae, Parvoviridae, Alloherpesviridae, Papillomaviridae). Interestingly, we also detected a 'core virome' that was shared by all the organs and was mainly composed of Caudovirales, Microviridae and Circoviridae. These results show that tuna host a mosaic of viral niches, whose establishment, role and circulation remain to be elucidated.

Microbial Shift in the Enteric Bacteriome of Coral Reef Fish Following Climate-Driven Regime Shifts.

Replacement of coral by macroalgae in post-disturbance reefs, also called a "coral-macroalgal regime shift", is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect on animal microbiota. In order to understand the consequence of coral-macroalgal shifts on the coral reef fish enteric bacteriome, we used a metabarcoding approach to examine the gut bacteriomes of 99 individual fish representing 36 species collected on reefs of the Inner Seychelles islands that, following bleaching, had either recovered to coral domination, or shifted to macroalgae. While the coral-macroalgal shift did not influence the diversity, richness or variability of fish gut bacteriomes, we observed a significant effect on the composition (R2 = 0.02; p = 0.001), especially in herbivorous fishes (R2 = 0.07; p = 0.001). This change is accompanied by a significant increase in the proportion of fermentative bacteria (Rikenella, Akkermensia, Desulfovibrio, Brachyspira) and associated metabolisms (carbohydrates metabolism, DNA replication, and nitrogen metabolism) in relation to the strong turnover of Scarinae and Siganidae fishes. Predominance of fermentative metabolisms in fish found on macroalgal dominated reefs indicates that regime shifts not only affect the taxonomic composition of fish bacteriomes, but also have the potential to affect ecosystem functioning through microbial functions.

Does the Composition of the Gut Bacteriome Change during the Growth of Tuna?

In recent years, a growing number of studies sought to examine the composition and the determinants of the gut microflora in marine animals, including fish. For tropical tuna, which are among the most consumed fish worldwide, there is scarce information on their enteric bacterial communities and how they evolve during fish growth. In this study, we used metabarcoding of the 16S rDNA gene to (1) describe the diversity and composition of the gut bacteriome in the three most fished tuna species (skipjack, yellowfin and bigeye), and (2) to examine its intra-specific variability from juveniles to larger adults. Although there was a remarkable convergence of taxonomic richness and bacterial composition between yellowfin and bigeyes tuna, the gut bacteriome of skipjack tuna was distinct from the other two species. Throughout fish growth, the enteric bacteriome of yellowfin and bigeyes also showed significant modifications, while that of skipjack tuna remained relatively homogeneous. Finally, our results suggest that the gut bacteriome of marine fish may not always be subject to structural modifications during their growth, especially in species that maintain a steady feeding behavior during their lifetime.

A community perspective on the concept of marine holobionts: current status, challenges, and future directions.

Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g., the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever.

Seasonality of archaeal proteorhodopsin and associated Marine Group IIb ecotypes (Ca. Poseidoniales) in the North Western Mediterranean Sea.

The Archaea Marine Group II (MGII) is widespread in the world's ocean where it plays an important role in the carbon cycle. Despite recent discoveries on the group's metabolisms, the ecology of this newly proposed order (Candidatus Poseidoniales) remains poorly understood. Here we used a combination of time-series metagenome-assembled genomes (MAGs) and high-frequency 16S rRNA data from the NW Mediterranean Sea to test if the taxonomic diversity within the MGIIb family (Candidatus Thalassarchaeaceae) reflects the presence of different ecotypes. The MAGs' seasonality revealed a MGIIb family composed of different subclades that have distinct lifestyles and physiologies. The vitamin metabolisms were notably different between ecotypes with, in some, a possible link to sunlight's energy. Diverse archaeal proteorhodopsin variants, with unusual signature in key amino acid residues, had distinct seasonal patterns corresponding to changing day length. In addition, we show that in summer, archaea, as opposed to bacteria, disappeared completely from surface waters. Our results shed light on the diversity and the distribution of the euryarchaeotal proteorhodopsin, and highlight that MGIIb is a diverse ecological group. The work shows that time-series based studies of the taxonomy, seasonality, and metabolisms of marine prokaryotes is critical to uncover their diverse role in the ocean.

Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes.

Coral reefs host hundreds of thousands of animal species that are increasingly threatened by anthropogenic disturbances. These animals host microbial communities at their surface, playing crucial roles for their fitness. However, the diversity of such microbiomes is mostly described in a few coral species and still poorly defined in other invertebrates and vertebrates. Given the diversity of animal microbiomes, and the diversity of host species inhabiting coral reefs, the contribution of such microbiomes to the total microbial diversity of coral reefs could be important, yet potentially vulnerable to the loss of animal species. Analysis of the surface microbiome from 74 taxa, including teleost fishes, hard and soft corals, crustaceans, echinoderms, bivalves and sponges, revealed that more than 90% of their prokaryotic phylogenetic richness was specific and not recovered in surrounding plankton. Estimate of the total richness associated with coral reef animal surface microbiomes reached up to 2.5% of current estimates of Earth prokaryotic diversity. Therefore, coral reef animal surfaces should be recognized as a hotspot of marine microbial diversity. Loss of the most vulnerable reef animals expected under present-day scenarios of reef degradation would induce an erosion of 28% of the prokaryotic richness, with unknown consequences on coral reef ecosystem functioning.

Resistance of the oyster pathogen Vibrio tasmaniensis LGP32 against grazing by Vannella sp. marine amoeba involves Vsm and CopA virulence factors.

Vibrios are ubiquitous in marine environments and opportunistically colonize a broad range of hosts. Strains of Vibrio tasmaniensis present in oyster farms can thrive in oysters during juvenile mortality events and behave as facultative intracellular pathogen of oyster haemocytes. Herein, we wondered whether V. tasmaniensis LGP32 resistance to phagocytosis is specific to oyster immune cells or contributes to resistance to other phagocytes, like marine amoebae. To address this question, we developed an integrative study, from the first description of amoeba diversity in oyster farms to the characterization of LGP32 interactions with amoebae. An isolate of the Vannella genus, Vannella sp. AP1411, which was collected from oyster farms, is ubiquitous, and belongs to one clade of Vannella that could be found associated with Vibrionaceae. LGP32 was shown to be resistant to grazing by Vannella sp. AP1411 and this phenotype depends on some previously identified virulence factors: secreted metalloprotease Vsm and copper efflux p-ATPase CopA, which act at different steps during amoeba-vibrio interactions, whereas some other virulence factors were not involved. Altogether, our work indicates that some virulence factors can be involved in multi-host interactions of V. tasmaniensis ranging from protozoans to metazoans, potentially favouring their opportunistic behaviour.

Geological gas-storage shapes deep life.

Around the world, several dozen deep sedimentary aquifers are being used for storage of natural gas. Ad hoc studies of the microbial ecology of some of them have suggested that sulfate reducing and methanogenic microorganisms play a key role in how these aquifers' communities function. Here, we investigate the influence of gas storage on these two metabolic groups by using high-throughput sequencing and show the importance of sulfate-reducing Desulfotomaculum and a new monophyletic methanogenic group. Aquifer microbial diversity was significantly related to the geological level. The distance to the stored natural gas affects the ratio of sulfate-reducing Firmicutes to deltaproteobacteria. In only one aquifer, the methanogenic archaea dominate the sulfate-reducers. This aquifer was used to store town gas (containing at least 50% H2 ) around 50 years ago. The observed decrease of sulfates in this aquifer could be related to stimulation of subsurface sulfate-reducers. These results suggest that the composition of the microbial communities is impacted by decades old transient gas storage activity. The tremendous stability of these gas-impacted deep subsurface microbial ecosystems suggests that in situ biotic methanation projects in geological reservoirs may be sustainable over time.

Genomic ecology of Marine Group II, the most common marine planktonic Archaea across the surface ocean.

Planktonic Archaea have been detected in all the world's oceans and are found from surface waters to the deep sea. The two most common Archaea phyla are Thaumarchaeota and Euryarchaeota. Euryarchaeota are generally more common in surface waters, but very little is known about their ecology and their potential metabolisms. In this study, we explore the genomic ecology of the Marine Group II (MGII), the main marine planktonic Euryarchaeota, and test if it is composed of different ecologically relevant units. We re-analyzed Tara Oceans metagenomes from the photic layer and the deep ocean by annotating sequences against a custom MGII database and by mapping gene co-occurrences. Our data provide a global view of the distribution of Euryarchaeota, and more specifically of MGII subgroups, and reveal their association to a number of gene-coding sequences. In particular, we show that MGII proteorhodopsins were detected in both the surface and the deep chlorophyll maximum layer and that different clusters of these light harvesting proteins were present. Our approach helped describing the set of genes found together with specific MGII subgroups. We could thus define genomic environments that could theoretically describe ecologically meaningful units and the ecological niche that they occupy.

Skin microbiome of coral reef fish is highly variable and driven by host phylogeny and diet.

BACKGROUND: The surface of marine animals is covered by abundant and diversified microbial communities, which have major roles for the health of their host. While such microbiomes have been deeply examined in marine invertebrates such as corals and sponges, the microbiomes living on marine vertebrates have received less attention. Specifically, the diversity of these microbiomes, their variability among species, and their drivers are still mostly unknown, especially among the fish species living on coral reefs that contribute to key ecosystem services while they are increasingly affected by human activities. Here, we investigated these knowledge gaps analyzing the skin microbiome of 138 fish individuals belonging to 44 coral reef fish species living in the same area. RESULTS: Prokaryotic communities living on the skin of coral reef fishes are highly diverse, with on average more than 600 OTUs per fish, and differ from planktonic microbes. Skin microbiomes varied between fish individual and species, and interspecific differences were slightly coupled to the phylogenetic affiliation of the host and its ecological traits. CONCLUSIONS: These results highlight that coral reef biodiversity is greater than previously appreciated, since the high diversity of macro-organisms supports a highly diversified microbial community. This suggest that beyond the loss of coral reefs-associated macroscopic species, anthropic activities on coral reefs could also lead to a loss of still unexplored host-associated microbial diversity, which urgently needs to be assessed.

A strong link between marine microbial community composition and function challenges the idea of functional redundancy.

Marine microbes have tremendous diversity, but a fundamental question remains unanswered: why are there so many microbial species in the sea? The idea of functional redundancy for microbial communities has long been assumed, so that the high level of richness is often explained by the presence of different taxa that are able to conduct the exact same set of metabolic processes and that can readily replace each other. Here, we refute the hypothesis of functional redundancy for marine microbial communities by showing that a shift in the community composition altered the overall functional attributes of communities across different temporal and spatial scales. Our metagenomic monitoring of a coastal northwestern Mediterranean site also revealed that diverse microbial communities harbor a high diversity of potential proteins. Working with all information given by the metagenomes (all reads) rather than relying only on known genes (annotated orthologous genes) was essential for revealing the similarity between taxonomic and functional community compositions. Our finding does not exclude the possibility for a partial redundancy where organisms that share some specific function can coexist when they differ in other ecological requirements. It demonstrates, however, that marine microbial diversity reflects a tremendous diversity of microbial metabolism and highlights the genetic potential yet to be discovered in an ocean of microbes.