Hydrothermal plumes as hotspots for deep-ocean heterotrophic microbial biomass production

Carbon budgets of hydrothermal plumes result from the balance between carbon sinks through plume chemoautotrophic processes and carbon release via microbial respiration. However, the lack of comprehensive analysis of the metabolic processes and biomass production rates hinders an accurate estimate of their contribution to the deep ocean carbon cycle. Here, we use a biogeochemical model to estimate the autotrophic and heterotrophic production rates of microbial communities in hydrothermal plumes and validate it with in situ data. We show how substrate limitation might prevent net chemolithoautotrophic production in hydrothermal plumes. Elevated prokaryotic heterotrophic production rates (up to 0.9 gCm−2y−1) compared to the surrounding seawater could lead to 0.05 GtCy−1 of C-biomass produced through chemoorganotrophy within hydrothermal plumes, similar to the Particulate Organic Carbon (POC) export fluxes reported in the deep ocean. We conclude that hydrothermal plumes must be accounted for as significant deep sources of POC in ocean carbon budgets.

Seasonal Prokaryotic Community Linkages Between Surface and Deep Ocean Water

Sinking organic particles from surface waters provide key nutrients to the deep ocean, and could serve as vectors transporting microbial diversity to the deep ocean. However, the effect of this seasonally varying connectivity with the surface on deep microbial communities remains unexplored. Here, a three-year time-series from surface and deep (500 m) waters part of the Munida Microbial Observatory Time-Series (MOTS) was used to study the seasonality of epipelagic and mesopelagic prokaryotic communities. The goal was to establish how seasonally dynamic these two communities are, and any potential linkages between them. Both surface and deep prokaryotic communities displayed seasonality with high variation in community diversity. Deep prokaryotic communities mirrored the seasonal patterns in heterotrophic production and bacterial abundance displayed by surface communities, which were related to changes in chlorophyll-a concentration. However, the magnitude of this temporal variability in deeper waters was generally smaller than in the surface. Detection of surface prokaryotes in the deep ocean seemed seasonally linked to phytoplankton blooms, but other copiotrophic or typically algal-associated surface groups were not detected in the mesopelagic suggesting only specific populations were surviving the migration down the water column. We show transfer of organisms across depths is possibly not always unidirectional, with typically deep ocean microbes being seasonally abundant in surface waters. This indicates the main mechanism linking surface and deep communities changes seasonally: sinking of organic particles during productive periods, and vertical convection during winter overturning.

Reviews and syntheses: Heterotrophic fixation of inorganic carbon – significant but invisible flux in environmental carbon cycling

Heterotrophic CO2 fixation is a significant yet underappreciated CO2 flux in environmental carbon cycling. In contrast to photosynthesis and chemolithoautotrophy – the main recognized autotrophic CO2 fixation pathways – the importance of heterotrophic CO2 fixation remains enigmatic. All heterotrophs – from microorganisms to humans – take up CO2 and incorporate it into their biomass. Depending on the availability and quality of growth substrates, and drivers such as the CO2 partial pressure, heterotrophic CO2 fixation contributes at least 1 %–5 % and in the case of methanotrophs up to 50 % of the carbon biomass. Assuming a standing stock of global heterotrophic biomass of 47–85 Pg C, we roughly estimate that up to 5 Pg C might be derived from heterotrophic CO2 fixation, and up to 12 Pg C yr−1 originating from heterotrophic CO2 fixation is funneled into the global annual heterotrophic production of 34–245 Pg C yr−1. These first estimates on the importance of heterotrophic fixation of inorganic carbon indicate that this pathway should be incorporated in present and future carbon cycling budgets.

Linking Microbial Functioning and Trophic Pathways to Ecological Status in a Coastal Mediterranean Ecosystem

Coastal marine ecosystems host complex microbial communities whose composition and metabolism are influenced by continental inputs and mesoscale properties of seawater masses. The identifying traits of the phytoplankton and bacteria such as biomass, size, shape and their metabolism related to organic matter production and degradation, recognized as indicators of the functioning of an ecosystem, were observed in the Gulf of Manfredonia (South Adriatic Sea, Italy) in late spring. This Gulf area is characterized by terrestrial inputs and mesoscale circulation influence such as coastal waters flowing southward from the North Adriatic and offshore waters interested by the Ionian Sea. Water samples were grouped in clusters (Coastal, Intermediate, Offshore and Deep Systems) according to the water column properties. Phytoplankton community biomass and composition, autotrophic and total prokaryotic abundances and microbial metabolism such as enzyme activity rates and prokaryotic heterotrophic production were analyzed to elucidate the trophic pathways with the objective to infer on the ecosystem status. As expected, size-fractionated phytoplankton biomass and production showed greater concentration in coastal waters with prevalence of the largest fractions (micro- and nano-) supported by the diatoms. Conversely, lower biomass and production were measured in all off-shore waters, mainly sustained by smallest fractions (nano-sized phytoflagellates and picophytoplankton). Total and autotrophic prokaryotic abundance decreased from coastal to offshore stations, inversely with respect to cell volume. Prokaryotic heterotrophic production was just below 50% compared to that of phytoplankton in all waters, evidencing an active biomass synthesis. High alkaline phosphatase and leucine aminopeptidase in coastal and offshore waters suggested the quick regeneration of Phosphorus and protein decomposition, respectively. Different levels of phytoplankton-bacteria association might provide a tool to define the ecological status of the studied system in the observed period; an approach to ecosystem assessment exportable to other coastal systems is proposed.

On the barium–oxygen consumption relationship in the Mediterranean Sea: implications for mesopelagic marine snow remineralization

In the ocean, remineralization rate associated with sinking particles is a crucial variable. Since the 1990s, particulate biogenic barium (Baxs) has been used as an indicator of carbon remineralization by applying a transfer function relating Baxs to O2 consumption (Dehairs's transfer function, Southern Ocean-based). Here, we tested its validity in the Mediterranean Sea (ANTARES/EMSO-LO) for the first time by investigating connections between Baxs, prokaryotic heterotrophic production (PHP) and oxygen consumption (JO2-Opt; optodes measurement). We show that (1) higher Baxs (409 pM; 100–500 m) occurs in situations where integrated PHP (PHP100/500=0.90) is located deeper, (2) higher Baxs occurs with increasing JO2-Opt, and (3) there is similar magnitude between JO2-Opt (3.14 mmol m−2 d−1; 175–450 m) and JO2-Ba (4.59 mmol m−2 d−1; transfer function). Overall, Baxs, PHP and JO2 relationships follow trends observed earlier in the Southern Ocean. We conclude that such a transfer function could apply in the Mediterranean Sea.

Reviews and syntheses: Heterotrophic fixation of inorganic carbon – significant but invisible flux in global carbon cycling

Heterotrophic CO2 fixation is a significant, yet underappreciated CO2 flux in the global carbon cycle. In contrast to photosynthesis and chemolithoautotrophy – the main recognized autotrophic CO2 fixation pathways – the importance of heterotrophic CO2 fixation remains enigmatic. All heterotrophs – from microorganisms to humans – take up CO2 and incorporate it into their biomass. Depending on the available growth substrates, heterotrophic CO2 fixation contributes at least 2–8 % and in the case of methanotrophs up to 50 % of the carbon building up their biomass. Assuming a standing stock of global heterotrophic biomass of 47–85 Pg C, we estimate that up to 7 Pg C have been derived from heterotrophic CO2 fixation and up to 20 Pg C yr−1 originating from heterotrophic CO2 fixation are funneled into the global annual heterotrophic production of 34–245 Pg C yr−1. These first estimates on the importance of heterotrophic fixation of inorganic carbon indicate that this carbon fixation pathway should be included in present and future global carbon budgets.

Particulate biogenic barium tracer of mesopelagic carbon remineralization in the Mediterranean Sea (PEACETIME project)

We report on the sub-basins variability of particulate organic carbon (POC) remineralization in the central and western Mediterranean Sea during a late spring period (PEACETIME cruise). POC remineralization rates (MR) were estimated using the excess non-lithogenic particulate barium (Baxs) inventories in mesopelagic waters (100–1000 m) and compared with prokaryotic heterotrophic production (PHP). MR range from 25 ± 2 to 306 ± 70 mg C m−2 d−1. Results reveal larger MR processes in the Algerian (ALG) basin compared to the Tyrrhenian (TYR) and Ionian (ION) basins. Baxs inventories and PHP also indicates that significant remineralization occurs over the whole mesopelagic layers in the ALG basin in contrast to the ION and TYR basins where remineralization is mainly located in the upper 500 m horizon. We propose that this may be due to particle injection pumps likely driven by strong winter convection in the Western basin of the Mediterranean Sea. This implies significant differences in the remineralization length scale of POC in the central Mediterranean Sea relative to the western region.

On the barium-oxygen consumption relationship in the Mediterranean Sea: implications for mesopelagic marine snow remineralisation

In the ocean, remineralisation rate associated with sinking particles is a crucial variable. Since the 90's, particulate biogenic barium (Baxs) has been used as an indicator of carbon remineralization by applying a transfer function relating Baxs to O2 consumption (Dehairs's transfer function, Southern Ocean-based). Here, we tested its validity in the Mediterranean Sea (ANTARES / EMSO-LO) for the first time by investigating connections between Baxs, prokaryotic heterotrophic production (PHP) and oxygen consumption (JO2-Opt; optodes measurement). We show that: (1) higher Baxs (409 pM; 100–500 m) in situations where integrated PHP (PHP100/500 = 0.90) is located deeper, (2) higher Baxs with increasing JO2-Opt, and (3) similar magnitude between JO2-Opt (3.14 mmol m−2 d−1; 175–450 m) and JO2-Ba (4.59 mmol m−2 d−1; transfer function). Overall, Baxs, PHP and JO2 relationships follow trends observed in the Southern Ocean. We believe that such transfer function could apply in the Mediterranean Sea with no restriction.

Assessing Viral Abundance and Community Composition in Four Contrasting Regions of the Southern Ocean

We explored how changes of viral abundance and community composition among four contrasting regions in the Southern Ocean relied on physicochemical and microbiological traits. During January–February 2015, we visited areas north and south of the South Orkney Islands (NSO and SSO) characterized by low temperature and salinity and high inorganic nutrient concentration, north of South Georgia Island (NSG) and west of Anvers Island (WA), which have relatively higher temperatures and lower inorganic nutrient concentrations. Surface viral abundance (VA) was highest in NSG (21.50 ± 10.70 × 106 viruses mL−1) and lowest in SSO (2.96 ± 1.48 × 106 viruses mL−1). VA was positively correlated with temperature, prokaryote abundance and prokaryotic heterotrophic production, chlorophyll a, diatoms, haptophytes, fluorescent organic matter, and isoprene concentration, and was negatively correlated with inorganic nutrients (NO3−, SiO42−, PO43−), and dimethyl sulfide (DMS) concentrations. Viral communities determined by randomly amplified polymorphic DNA–polymerase chain reaction (RAPD-PCR) were grouped according to the sampling location, being more similar within them than among regions. The first two axes of a canonical correspondence analysis, including physicochemical (temperature, salinity, inorganic nutrients—NO3−, SiO42−, and dimethyl sulfoniopropionate -DMSP- and isoprene concentrations) and microbiological (chlorophyll a, haptophytes and diatom, and prokaryote abundance and prokaryotic heterotrophic production) factors accounted for 62.9% of the variance. The first axis, temperature-related, accounted for 33.8%; the second one, salinity-related, accounted for 29.1%. Thus, different environmental situations likely select different hosts for viruses, leading to distinct viral communities.