Microbial biodiversity and viral impact in benthic deep-sea ecosystems

Gli ambienti marini profondi ricoprono il 95% del globo terrestre e sono caratterizzati da basse temperature, assenza di luce ed elevate pressioni. Tra i sistemi marini profondi i più remoti e inesplorati sono le fosse adali, sistemi che possono superare gli 11000 m di profondità. Lo studio di questi ambienti estremi rappresenta una delle più grandi sfide della ricerca scientifica a causa delle difficoltà che si presentano nel raggiungerli. Questo studio fornisce i primi dati riguardanti l’impatto dei virus sui procarioti che abitano i sedimenti di tre tra le più profonde fosse oceaniche conosciute, Japan, Ogasawara e Mariana. In questo studio abbiamo esplorato il ruolo dei virus come agenti di mortalità procariotica, in grado di influenzare i cicli di C e nutrienti tramite la lisi cellulare dei loro ospiti contribuendo così al funzionamento delle reti trofiche microbiche e al funzionamento ecosistemico degli ambienti profondi. I nostri risultati rivelano che tutte le fosse adali qui investigate supportano elevate abbondanze e biomasse procariotiche favorendo alti tassi di lisi virale e stimolando il rilascio di materia organica resa così disponibile per le comunità bentoniche. Specialmente nella fossa Mariana la lisi virale è potenzialmente esercitata con maggiore pressione sui taxa microbici dominanti influenzando la struttura della rete trofica microbica e i cicli di C e N, e contribuendo così all’elevato metabolismo procariotico precedentemente riconosciuto in questi sistemi ultra abissali. Oltre alle interazioni microbiche, in questo studio è stata esplorata la diversità delle comunità procariotiche presenti nelle fosse investigate ed è stato determinato l’importante contributo della componente archaeale alla struttura di queste comunità. Il predominio di archaea ammonio-ossidanti suggerisce che i processi chemoautotrofici presentano un ruolo chiave per il funzionamento delle fosse adali. Inoltre, l’elevato numero di taxa, ritrovato specialmente nella fossa Japan, rivela che gli ecosistemi delle fosse adali possono rappresentare hot spot di diversità procariotica. In aggiunta, la presenza di taxa procariotici diffusi in habitat abissali bentonici suggerisce che le fosse adali sono solo parzialmente connesse agli ecosistemi bentonici circostanti. In questo studio abbiamo anche investigato le risposte, su diverse scale temporali, delle comunità microbiche abissali (interazioni virus-procarioti e diversità batterica) all’impatto dell’attività di estrazione di risorse minerarie, che rappresenta una delle future minacce tra le più impattanti per questi ambienti. I risultati ottenuti indicano un aumento dei tassi d’infezione virale sulla componente batterica potenzialmente dovuto ad una cambiamento della composizione in specie di tale componente a seguito dell’attività di mining, anche molti anni dopo l’impatto e con potenziali conseguenze sui cicli biogeochimici e sul funzionamento ecosistemico bentonico.Deep-sea ecosystems cover 95% of the entire globe and are characterized by low temperature, absence of solar radiation, and elevate pressures. Among the deep-sea environments the most remote and unexplored habitats are the hadal trenches, ultra-abyssal systems exceeding also 11000 m depth. Their study represents one of the greatest challenges of the scientific research, due to the high difficulties in reaching such remote habitats. This study presents the first data on virus-prokaryote interactions within the benthic microbial assemblages inhabiting three of the deepest known ocean trenches, Japan, Ogasawara and Mariana Trench. Here, we evaluated the role of viruses as agents of prokaryotic mortality and in influencing the C and nutrient cycles through the cell lysis of their hosts thus contributing to the functioning of the deep-sea microbial food-webs and biogeochemical cycles. Our results reveal that all hadal trenches investigated support high prokaryotic abundances and biomasses favouring high rates of viral lysis and stimulating the release of highly bioavailable organic matter for benthic metabolism. Especially, in the Mariana Trench the viral pressure is likely to be preferentially exerted on the dominant microbial taxa, thus influencing the structure of the microbial food webs and C and N cycling and contributing to explain the high microbial metabolism previously reported in this ultra abyssal ecosystem. In this study, we also investigated the community structure and diversity of prokaryotic assemblages inhabiting the studied trenches. We found a relevant contribution of archaea to trenches’ microbial communities and the predominance of ammonia oxidizers suggesting the key role of chemoautotrophic processes in the functioning of hadal trenches. Moreover, the high prokaryotic richness found, especially at the bottom of the Japan Trench, highlights that hadal ecosystems can be potential hot spot of microbial biodiversity. In addition, the presence within the hadal sediments of prokaryotic taxa found in abyssal habitats leads to hypothesize that hadal trenches are only partially connected to the surrounding benthic ecosystems. In this study, we have also investigated the responses at different time scales of deep-sea microbial assemblages (virus-prokaryote interactions and bacterial diversity) to anthropogenic impact due to mineral exploitation, which will represent a major future threat for deep-sea habitats. The results obtained indicate an increase of viral lysis rates potentially due to a shift in the composition of bacterial assemblages after the mining activity even several years after the impact, with potential consequences on biogeochemical cycles and functioning of the benthic microbial food webs

Modelling distribution and fate of coralligenous habitat in the Northern Adriatic Sea under a severe climate change scenario

Due to their well-acknowledged capability in predicting habitat distributions, Habitat Suitability Models (HSMs) are particularly useful for investigating ecological patterns variations under climate change scenarios. The shallow coastal regions of the Northern Adriatic Sea, a sub-basin of the Mediterranean Sea, are studded with coralligenous outcrops recognized as important biodiversity hotspots exposed to the effects of climate change. In this research, we investigate the distributions of the Northern Adriatic Sea coralligenous habitats characterized by diverse species assemblages differently influenced by environmental factors, and provide a projection of how these might be impacted by climate change. Two models (Random Forest and MaxEnt), populated with occurrence data gathered from previous publications, environmental parameters’ from online databases (CMEMS, Bio-Oracle), and a set of dedicated ocean model simulations, are applied in recent past conditions and under a future severe climate change scenario (RCP 8.5). The model performance metrics confirm the ability of both approaches for predicting habitat distribution and their relationship with environmental conditions. The results show that salinity, temperature, and nitrate concentration are generally the most relevant variables in affecting the coralligenous outcrops distribution. The environmental variations projected under climate change conditions are expected to favour the spreading of opportunistic organisms, more tolerant to stressful conditions, at the expense of more vulnerable species. This will result in a shift in the distribution of these habitats, with a consequent potential loss of biodiversity in the Northern Adriatic Sea

Abyssal fauna, benthic microbes, and organic matter quality across a range of trophic conditions in the western Pacific ocean

Abstract The abyssal plain covers more than half the Earth's surface. The main food source to abyssal ecosystems is phytodetritus, which originates from phytoplankton in the surface ocean, and thus its variability to the seafloor is a major driver of abyssal ecosystem biomass and functioning. In this study, we conducted a comparative survey on organic matter (OM) quality and quantity in abyssal plain sediments and examined the distributions of megafauna, macrofauna, meiofauna, prokaryotes, and viruses in eutrophic (39°N), oligotrophic (1°N), and ultra-oligotrophic (12°N) areas of the western Pacific. We also analyzed stable carbon and nitrogen isotopic compositions of organisms at 39°N and 1°N to assess differences in benthic abyssal food-web structures with contrasting trophic states. Sediments collected at 39°N presented highest concentrations of total organic carbon (TOC) and labile OM, and high diffusive oxygen uptake rates. By contrast, the lowest values were found at 12°N. Vertical distributions of sediment macrofauna, meiofauna, and prokaryotes matched with labile OM profiles. There were prominent differences in abundances of macro- and megafauna among stations with different OM fluxes, whereas the abundance of meiofauna and prokaryotes showed smaller differences among stations. Such differences could be explained by higher turnover rates of smaller organisms. Food-web structures of abyssal plains are likely influenced by both the type and size of primary producers in surface ocean. Our results underscore the crucial importance of OM fluxes and their compositions to the abundances and vertical profiles of labile OM and benthic biota in abyssal ecosystems

Are we overlooking Natura 2000 sites? Lessons learned from a transnational project in the Adriatic Sea

Since the adoption of the Habitats and Birds Directives by EU governments, marine Natura 2000 (N2K) sites have been established in the European Mediterranean Sea, creating one of the largest international networks of protected areas. Nevertheless, to date, marine N2K sites are generally scarcely implemented, studied and monitored, and thus their management effectiveness is weak, and their environmental status is often unknown. The Interreg Italy-Croatia ECOSS project aimed at establishing the ECOlogical observing system of the Adriatic Sea (ECOAdS), to integrate the existing research and monitoring activities in the area, and to promote data sharing at international level, for enhancing monitoring and conservation in Adriatic N2K network. In the framework of ECOSS, a conceptual model was developed and applied to selected N2K sites, to review the existing knowledge, assess site effectiveness, and suggest possible improvements in their monitoring and management based on the contribution that ECOAdS can provide to their implementation. Information on social, ecological, and oceanographic elements related to the conservation and management of these case studies was gathered by consulting the project partners involved in the management and monitoring of the sites and through a literature review. The results of this study revealed a discouraging condition with no management plan in most of the sites, while regulatory measures are generally in place but without surveillance. Monitoring activities are performed occasionally, and information on presence and status of protected species is often lacking or outdated. Although the N2K network provides a unique opportunity to advance marine conservation and achieve the 30% conservation target by 2030, the biggest challenge ahead is the proper management and monitoring of N2K sites. The proposed conceptual model may be taken as a framework to properly set up ecological observing systems in the N2K network and help overcome current limitations, integrating scientific research within the N2K conservation strategies

Framing Cutting-Edge Integrative Deep-Sea Biodiversity Monitoring via Environmental DNA and Optoacoustic Augmented Infrastructures

17 pages, 1 figure, 1 tableDeep-sea ecosystems are reservoirs of biodiversity that are largely unexplored, but their exploration and biodiscovery are becoming a reality thanks to biotechnological advances (e.g., omics technologies) and their integration in an expanding network of marine infrastructures for the exploration of the seas, such as cabled observatories. While still in its infancy, the application of environmental DNA (eDNA) metabarcoding approaches is revolutionizing marine biodiversity monitoring capability. Indeed, the analysis of eDNA in conjunction with the collection of multidisciplinary optoacoustic and environmental data, can provide a more comprehensive monitoring of deep-sea biodiversity. Here, we describe the potential for acquiring eDNA as a core component for the expanding ecological monitoring capabilities through cabled observatories and their docked Internet Operated Vehicles (IOVs), such as crawlers. Furthermore, we provide a critical overview of four areas of development: (i) Integrating eDNA with optoacoustic imaging; (ii) Development of eDNA repositories and cross-linking with other biodiversity databases; (iii) Artificial Intelligence for eDNA analyses and integration with imaging data; and (iv) Benefits of eDNA augmented observatories for the conservation and sustainable management of deep-sea biodiversity. Finally, we discuss the technical limitations and recommendations for future eDNA monitoring of the deep-sea. It is hoped that this review will frame the future direction of an exciting journey of biodiscovery in remote and yet vulnerable areas of our planet, with the overall aim to understand deep-sea biodiversity and hence manage and protect vital marine resourcesThis research has been funded within the framework of the following project activities: ARIM (Autonomous Robotic Sea-Floor Infrastructure for Benthopelagic Monitoring; MarTERA ERA-Net Cofound); RESBIO (TEC2017-87861-R; Ministerio de Ciencia, Innovación y Universidades); JERICO-S3: (Horizon 2020; Grant Agreement no. 871153); ENDURUNS (Research Grant Agreement H2020-MG-2018-2019-2020 n.824348); Slovenian Research Agency (Research Core Funding Nos. P1-0237 and P1-0255 and project ARRS-RPROJ-JR-J1-3015). We also profited of the funding from the Spanish Government through the “Severo Ochoa Centre of Excellence” accreditation (CEX2019-000928-S) and Italian Ministry of Education (MIUR) under the “Bando premiale FOE 2015” (nota prot. N. 850, dd. 27 ottobre 2017) with the project EarthCruisers “EARTH’s CRUst Imagery for Investigating Seismicity, Volcanism, and Marine Natural Resources in the Sicilian Offshore”. Ocean Networks Canada was funded through Canada Foundation for Innovation-Major Science Initiative (CFI-MSI) fund 30199Peer reviewe

Framing Cutting-Edge Integrative Deep-Sea Biodiversity Monitoring via Environmental DNA and Optoacoustic Augmented Infrastructures

Deep-sea ecosystems are reservoirs of biodiversity that are largely unexplored, but their exploration and biodiscovery are becoming a reality thanks to biotechnological advances (e.g., omics technologies) and their integration in an expanding network of marine infrastructures for the exploration of the seas, such as cabled observatories. While still in its infancy, the application of environmental DNA (eDNA) metabarcoding approaches is revolutionizing marine biodiversity monitoring capability. Indeed, the analysis of eDNA in conjunction with the collection of multidisciplinary optoacoustic and environmental data, can provide a more comprehensive monitoring of deep-sea biodiversity. Here, we describe the potential for acquiring eDNA as a core component for the expanding ecological monitoring capabilities through cabled observatories and their docked Internet Operated Vehicles (IOVs), such as crawlers. Furthermore, we provide a critical overview of four areas of development: (i) Integrating eDNA with optoacoustic imaging ; (ii) Development of eDNA repositories and cross-linking with other biodiversity databases ; (iii) Artificial Intelligence for eDNA analyses and integration with imaging data ; and (iv) Benefits of eDNA augmented observatories for the conservation and sustainable management of deep-sea biodiversity. Finally, we discuss the technical limitations and recommendations for future eDNA monitoring of the deep-sea. It is hoped that this review will frame the future direction of an exciting journey of biodiscovery in remote and yet vulnerable areas of our planet, with the overall aim to understand deep-sea biodiversity and hence manage and protect vital marine resources

An integrated assessment of the Good Environmental Status of Mediterranean Marine Protected Areas

Este artículo contiene 11 páginas, 2 figuras, 2 tablas.Local, regional and global targets have been set to halt marine biodiversity loss. Europe has set its own policy targets to achieve Good Environmental Status (GES) of marine ecosystems by implementing the Marine Strategy Framework Directive (MSFD) across member states. We combined an extensive dataset across five Mediterranean ecoregions including 26 Marine Protected Areas (MPAs), their reference unprotected areas, and a no-trawl case study. Our aim was to assess if MPAs reach GES, if their effects are local or can be detected at ecoregion level or up to a Mediterranean scale, and which are the ecosystem components driving GES achievement. This was undertaken by using the analytical tool NEAT (Nested Environmental status Assessment Tool), which allows an integrated assessment of the status of marine systems. We adopted an ecosystem approach by integrating data from several ecosystem components: the seagrass Posidonia oceanica, macroalgae, sea urchins and fish. Thresholds to define the GES were set by dedicated workshops and literature review. In the Western Mediterranean, most MPAs are in good/high status, with P. oceanica and fish driving this result within MPAs. However, GES is achieved only at a local level, and the Mediterranean Sea, as a whole, results in a moderate environmental status. Macroalgal forests are overall in bad condition, confirming their status at risk. The results are significantly affected by the assumption that discrete observations over small spatial scales are representative of the total extension investigated. This calls for large-scale, dedicated assessments to realistically detect environmental status changes under different conditions. Understanding MPAs effectiveness in reaching GES is crucial to assess their role as sentinel observatories of marine systems. MPAs and trawling bans can locally contribute to the attainment of GES and to the fulfillment of the MSFD objectives. Building confidence in setting thresholds between GES and non-GES, investing in long-term monitoring, increasing the spatial extent of sampling areas, rethinking and broadening the scope of complementary tools of protection (e.g., Natura 2000 Sites), are indicated as solutions to ameliorate the status of the basin.This article was undertaken within the COST Action 15121 MarCons (http://www.marcons-cost.eu, European Cooperation in Science and Technology), the Interreg MED AMAre Plus (Ref: 8022) and the project PO FEAMP 2014-2020 Innovazione, sviluppo e sostenibilita ` nel settore della pesca e dell’acquacoltura per la Regione Campania (ISSPA 2.51). M.C.U., A.B. have been funded by the project MEDREGION (European Commission DG ENV/MSFD, 2018 call, Grant Agreement 110661/ 2018/794286/SUB/ENV.C2). Aegean Sea data were retrieved from the project PROTOMEDEA (www.protomedea.eu), funded by DG for Marine Affairs and Fisheries of the EC, under Grant Agreement SI2.721917. JB acknowledges support from the Spanish Ministry of Science and Innovation (Juan de la Cierva fellowship FJC 2018-035566-I).With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S).Peer reviewe

A blueprint for an inclusive, global deep-sea Ocean Decade field programme

The ocean plays a crucial role in the functioning of the Earth System and in the provision of vital goods and services. The United Nations (UN) declared 2021–2030 as the UN Decade of Ocean Science for Sustainable Development. The Roadmap for the Ocean Decade aims to achieve six critical societal outcomes (SOs) by 2030, through the pursuit of four objectives (Os). It specifically recognizes the scarcity of biological data for deep-sea biomes, and challenges the global scientific community to conduct research to advance understanding of deep-sea ecosystems to inform sustainable management. In this paper, we map four key scientific questions identified by the academic community to the Ocean Decade SOs: (i) What is the diversity of life in the deep ocean? (ii) How are populations and habitats connected? (iii) What is the role of living organisms in ecosystem function and service provision? and (iv) How do species, communities, and ecosystems respond to disturbance? We then consider the design of a global-scale program to address these questions by reviewing key drivers of ecological pattern and process. We recommend using the following criteria to stratify a global survey design: biogeographic region, depth, horizontal distance, substrate type, high and low climate hazard, fished/unfished, near/far from sources of pollution, licensed/protected from industry activities. We consider both spatial and temporal surveys, and emphasize new biological data collection that prioritizes southern and polar latitudes, deeper (> 2000 m) depths, and midwater environments. We provide guidance on observational, experimental, and monitoring needs for different benthic and pelagic ecosystems. We then review recent efforts to standardize biological data and specimen collection and archiving, making “sampling design to knowledge application” recommendations in the context of a new global program. We also review and comment on needs, and recommend actions, to develop capacity in deep-sea research; and the role of inclusivity - from accessing indigenous and local knowledge to the sharing of technologies - as part of such a global program. We discuss the concept of a new global deep-sea biological research program ‘Challenger 150,’ highlighting what it could deliver for the Ocean Decade and UN Sustainable Development Goal 14

Microbial biodiversity and viral impact in benthic deep-sea ecosystems

Gli ambienti marini profondi ricoprono il 95% del globo terrestre e sono caratterizzati da basse temperature, assenza di luce ed elevate pressioni. Tra i sistemi marini profondi i più remoti e inesplorati sono le fosse adali, sistemi che possono superare gli 11000 m di profondità. Lo studio di questi ambienti estremi rappresenta una delle più grandi sfide della ricerca scientifica a causa delle difficoltà che si presentano nel raggiungerli. Questo studio fornisce i primi dati riguardanti l’impatto dei virus sui procarioti che abitano i sedimenti di tre tra le più profonde fosse oceaniche conosciute, Japan, Ogasawara e Mariana. In questo studio abbiamo esplorato il ruolo dei virus come agenti di mortalità procariotica, in grado di influenzare i cicli di C e nutrienti tramite la lisi cellulare dei loro ospiti contribuendo così al funzionamento delle reti trofiche microbiche e al funzionamento ecosistemico degli ambienti profondi. I nostri risultati rivelano che tutte le fosse adali qui investigate supportano elevate abbondanze e biomasse procariotiche favorendo alti tassi di lisi virale e stimolando il rilascio di materia organica resa così disponibile per le comunità bentoniche. Specialmente nella fossa Mariana la lisi virale è potenzialmente esercitata con maggiore pressione sui taxa microbici dominanti influenzando la struttura della rete trofica microbica e i cicli di C e N, e contribuendo così all’elevato metabolismo procariotico precedentemente riconosciuto in questi sistemi ultra abissali. Oltre alle interazioni microbiche, in questo studio è stata esplorata la diversità delle comunità procariotiche presenti nelle fosse investigate ed è stato determinato l’importante contributo della componente archaeale alla struttura di queste comunità. Il predominio di archaea ammonio-ossidanti suggerisce che i processi chemoautotrofici presentano un ruolo chiave per il funzionamento delle fosse adali. Inoltre, l’elevato numero di taxa, ritrovato specialmente nella fossa Japan, rivela che gli ecosistemi delle fosse adali possono rappresentare hot spot di diversità procariotica. In aggiunta, la presenza di taxa procariotici diffusi in habitat abissali bentonici suggerisce che le fosse adali sono solo parzialmente connesse agli ecosistemi bentonici circostanti. In questo studio abbiamo anche investigato le risposte, su diverse scale temporali, delle comunità microbiche abissali (interazioni virus-procarioti e diversità batterica) all’impatto dell’attività di estrazione di risorse minerarie, che rappresenta una delle future minacce tra le più impattanti per questi ambienti. I risultati ottenuti indicano un aumento dei tassi d’infezione virale sulla componente batterica potenzialmente dovuto ad una cambiamento della composizione in specie di tale componente a seguito dell’attività di mining, anche molti anni dopo l’impatto e con potenziali conseguenze sui cicli biogeochimici e sul funzionamento ecosistemico bentonico.Deep-sea ecosystems cover 95% of the entire globe and are characterized by low temperature, absence of solar radiation, and elevate pressures. Among the deep-sea environments the most remote and unexplored habitats are the hadal trenches, ultra-abyssal systems exceeding also 11000 m depth. Their study represents one of the greatest challenges of the scientific research, due to the high difficulties in reaching such remote habitats. This study presents the first data on virus-prokaryote interactions within the benthic microbial assemblages inhabiting three of the deepest known ocean trenches, Japan, Ogasawara and Mariana Trench. Here, we evaluated the role of viruses as agents of prokaryotic mortality and in influencing the C and nutrient cycles through the cell lysis of their hosts thus contributing to the functioning of the deep-sea microbial food-webs and biogeochemical cycles. Our results reveal that all hadal trenches investigated support high prokaryotic abundances and biomasses favouring high rates of viral lysis and stimulating the release of highly bioavailable organic matter for benthic metabolism. Especially, in the Mariana Trench the viral pressure is likely to be preferentially exerted on the dominant microbial taxa, thus influencing the structure of the microbial food webs and C and N cycling and contributing to explain the high microbial metabolism previously reported in this ultra abyssal ecosystem. In this study, we also investigated the community structure and diversity of prokaryotic assemblages inhabiting the studied trenches. We found a relevant contribution of archaea to trenches’ microbial communities and the predominance of ammonia oxidizers suggesting the key role of chemoautotrophic processes in the functioning of hadal trenches. Moreover, the high prokaryotic richness found, especially at the bottom of the Japan Trench, highlights that hadal ecosystems can be potential hot spot of microbial biodiversity. In addition, the presence within the hadal sediments of prokaryotic taxa found in abyssal habitats leads to hypothesize that hadal trenches are only partially connected to the surrounding benthic ecosystems. In this study, we have also investigated the responses at different time scales of deep-sea microbial assemblages (virus-prokaryote interactions and bacterial diversity) to anthropogenic impact due to mineral exploitation, which will represent a major future threat for deep-sea habitats. The results obtained indicate an increase of viral lysis rates potentially due to a shift in the composition of bacterial assemblages after the mining activity even several years after the impact, with potential consequences on biogeochemical cycles and functioning of the benthic microbial food webs

Towards a global strategy for the conservation of deep-sea active hydrothermal vents

Abstract Deep-sea active hydrothermal vents are globally diverse, vulnerable, rare, remote, and isolated habitats, yet they face increasing threats from human activities, including deep-sea mining. To address the conservation challenges surrounding these habitats, we present a global assessment of the conservation status of deep-sea active vents. Our findings reveal that while 25% of the known deep active hydrothermal vents are currently under conservation interventions, only 8% benefit of full protection. These conservation interventions, consisting of area-based and regulation-based management measures, are implemented by 17 Sovereign States, three Regional Fisheries Management Organizations and one international treaty through 30 discrete interventions. However, our assessment and comparison of the specific measures for the 155 managed active hydrothermal vents reveal that the current conservation remain fragmented and discordant across jurisdictions and biogeographical provinces, resulting in overall insufficient protection, especially in Areas Beyond National Jurisdiction. Seizing the current momentum for ocean conservation, it is crucial to harmonize the management and protection of active deep-sea vents worldwide, taking into account their global biogeographic context and spatial distribution. This requires aligning current international initiatives that could improve baseline policies for the global protection of deep-sea hydrothermal vents