ABSTRACT
The Proterozoic Era records two periods of abundant positive carbon isotope excursions (CIEs), conventionally interpreted as resulting from increased organic carbon burial and leading to Earth's surface oxygenation. As strong spatial variations in the amplitude and duration of these excursions are uncovered, this interpretation is challenged. Here, by studying the carbon cycle in the Dziani Dzaha Lake, we propose that they could be due to regionally variable methane emissions to the atmosphere. This lake presents carbon isotope signatures deviated by ~ + 12 compared to the modern ocean and shares a unique combination of analogies with putative Proterozoic lakes, interior seas or restricted epireic seas. A simple box model of its Carbon cycle demonstrates that its current isotopic signatures are due to high primary productivity, efficiently mineralized by methanogenesis, and to subsequent methane emissions to the atmosphere. By analogy, these results might allow the reinterpretation of some positive CIEs as at least partly due to regionally large methane emissions. This supports the view that methane may have been a major greenhouse gas during the Proterozoic Era, keeping the Earth from major glaciations, especially during periods of positive CIEs, when increased organic carbon burial would have drowned down atmospheric CO2.
ABSTRACT
Phytoplankton and bacterioplankton are the key components of the organic matter cycle in aquatic ecosystems, and their interactions can impact the transfer of carbon and ecosystem functioning. The aim of this work was to assess the consequences of chemical contamination on the coupling between phytoplankton and bacterioplankton in two contrasting marine coastal ecosystems: lagoon waters and offshore waters. Bacterial carbon demand was sustained by primary carbon production in the offshore situation, suggesting a tight coupling between both compartments. In contrast, in lagoon waters, due to a higher nutrient and organic matter availability, bacteria could rely on allochthonous carbon sources to sustain their carbon requirements, decreasing so the coupling between both compartments. Exposure to chemical contaminants, pesticides and metal trace elements, resulted in a significant inhibition of the metabolic activities (primary production and bacterial carbon demand) involved in the carbon cycle, especially in offshore waters during spring and fall, inducing a significant decrease of the coupling between primary producers and heterotrophs. This coupling loss was even more evident upon sediment resuspension for both ecosystems due to the important release of nutrients and organic matter. Resulting enrichment alleviated the toxic effects of contaminants as indicated by the stimulation of phytoplankton biomass and carbon production, and modified the composition of the phytoplankton community, impacting so the interactions between phytoplankton and bacterioplankton.
Subject(s)
Phytoplankton/physiology , Water Pollutants, Chemical/toxicity , Bacteria/metabolism , Biomass , Carbon/metabolism , Ecosystem , Pesticides/metabolism , Seasons , Seawater/chemistry , Trace Elements/metabolismABSTRACT
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
ABSTRACT
Positive interactions such as facilitation play an important role during the biological colonization and species succession in harsh or changing environments. However, the direct evidence of such ecological interaction in microbial communities remains rare. Using common freshwater microalgae isolated from a High Rate Algal Pond HRAP treating wastewaters, we investigated with both experimental and modeling approaches the direct facilitation between two algal strains during the colonization phase. Our results demonstrate that the first colonization by microalgae under a severe chemical condition arose from the rapid growth of pioneer species such as Chlorella sorokiniana, which facilitated the subsequent colonization of low growth specialists such as Scenedesmus pectinatus. The pioneer species rapidly depleted the total available ammonia nitrogen favoring the specialist species initially inhibited by free ammonia toxicity. This latter species ultimately dominated the algal community through competitive exclusion under low nutrient conditions. We show that microbial successions are not only regulated by climatic conditions but also by interactions between species based on the ability to modify their growth conditions. We suggest that facilitation within the aquatic microbial communities is a widespread ecological interaction under a vast range of environmental stress.
Subject(s)
Chlorella/growth & development , Microalgae/growth & development , Scenedesmus/growth & development , Stress, Physiological , Wastewater/microbiology , Water Microbiology , Water PurificationABSTRACT
When microalgae are exposed to contaminants, the role of associated bacteria within the phycosphere, the microenvironment surrounding algal cells, remains largely unknown. The present study investigated the importance of algae-associated bacteria on the responses of microalgae growth to metallic and organic toxicant exposure. The effects of a polluted sediment elutriate, and of metal or pesticide mixtures at environmentally relevant concentrations (<10⯵gâ¯L-1) were assessed on the growth of two microalgae strains: Isochrysis galbana, a prymnesiophyte, and Thalassiosira delicatula, a centric diatom. Both cultures were maintained as axenic or bacterized under similar conditions in batch cultures. In axenic conditions, the metal mixture addition at low concentrations alleviated limitation of growth by metals for T. delicatula relative to control, but inhibited I. galbana growth at highest concentration. In similar axenic conditions, both T. delicatula and I. galbana growth were negatively inhibited by pesticide mixture at concentrations as low as 10â¯ngâ¯L-1. The bacterial diversities associated with the two microalgae strains were significantly different (Bray-Curtis dissimilarity greater than 0.9) but their impact on microalgae growth was similar. The presence of bacteria reduced algal growth rate by ca. 50% compared to axenic cultures, whereas no significant effect of sediment elutriate, metal or pesticide mixtures was noticed on non-axenic algal growth rates. These results show that bacteria may have a negative effect on algal growth but can reduce pesticide toxicity or metal availability to algae.
Subject(s)
Bacteria/pathogenicity , Geologic Sediments/chemistry , Microalgae/drug effectsABSTRACT
Recent observations in polar marine waters have shown that a large fraction of primary production may be lost to respiration by planktonic bacteria due to very low bacterial growth efficiencies in cold waters. Here we report that sea temperature may be a key factor (but not the only one) influencing the interaction between bacteria and primary production in North Atlantic and Arctic waters, suggesting that low primary production rates could not sustain bacterial carbon demand in the coldest Arctic waters. The use of freshly produced phytoplankton exudate by bacteria in early- and mid-summer was assessed, together with the bacterial uptake of dissolved inorganic nitrogen (DIN = nitrate and ammonium), in surface waters along a latitudinal gradient from the North Sea to the Arctic sea ice. Bacterial production was independent of the low primary production measured in the coldest waters. Under these conditions, heterotrophic bacteria can consume a large fraction of DIN and N-rich organic matter, making them strong contributors to N fluxes in these waters.
Subject(s)
Bacteria/growth & development , Phytoplankton/growth & development , Seawater/microbiology , Arctic Regions , Bacteria/metabolism , Carbon/metabolism , Heterotrophic Processes , Microbial Interactions , Nitrogen/metabolism , North Sea , Phytoplankton/metabolism , SeasonsABSTRACT
This study describes, for the first time, the water chemistry and microbial diversity in Dziani Dzaha, a tropical crater lake located on Mayotte Island (Comoros archipelago, Western Indian Ocean). The lake water had a high level of dissolved matter and high alkalinity (10.6-14.5 g L-1 eq. CO32-, i.e. 160-220 mM compare to around 2-2.5 in seawater), with salinity up to 52 psu, 1.5 higher than seawater. Hierarchical clustering discriminated Dziani Dzaha water from other alkaline, saline lakes, highlighting its thalassohaline nature. The phytoplankton biomass was very high, with a total chlorophyll a concentration of 524 to 875 µg chl a L-1 depending on the survey, homogeneously distributed from surface to bottom (4 m). Throughout the whole water column the photosynthetic biomass was dominated (>97% of total biovolume) by the filamentous cyanobacteria Arthrospira sp. with a straight morphotype. In situ daily photosynthetic oxygen production ranged from 17.3 to 22.2 g O2 m-2 d-1, consistent with experimental production / irradiance measurements and modeling. Heterotrophic bacterioplankton was extremely abundant, with cell densities up to 1.5 108 cells mL-1 in the whole water column. Isolation and culture of 59 Eubacteria strains revealed the prevalence of alkaliphilic and halophilic organisms together with taxa unknown to date, based on 16S rRNA gene analysis. A single cloning-sequencing approach using archaeal 16S rDNA gene primers unveiled the presence of diverse extremophilic Euryarchaeota. The water chemistry of Dziani Dzaha Lake supports the hypothesis that it was derived from seawater and strongly modified by geological conditions and microbial activities that increased the alkalinity. Dziani Dzaha has a unique consortium of cyanobacteria, phytoplankton, heterotrophic Eubacteria and Archaea, with very few unicellular protozoa, that will deserve further deep analysis to unravel its uncommon diversity. A single taxon, belonging to the genus Arthrospira, was found responsible for almost all photosynthetic primary production.
Subject(s)
Biodiversity , Cyanobacteria , Lakes/microbiology , Water Microbiology , Biomass , Carbon/chemistry , Chlorophyll/metabolism , Chlorophyll A , Cluster Analysis , Comoros , Geography , Hydrogen-Ion Concentration , Islands , Models, Statistical , Nitrogen/chemistry , Oxygen/analysis , Oxygen/chemistry , Photosynthesis , Phytoplankton , Principal Component Analysis , RNA, Ribosomal, 16S/metabolism , TemperatureABSTRACT
This work describes a method to model the optical properties over the (400-750 nm) spectral range of a dense microalgal culture using the chemical and physical properties of the algal cells. The method was based on a specific program called AlgaSim coupled with the adding-doubling method: at the individual cell scale, AlgaSim simulates the spectral properties of one model, three-layer spherical algal cell from its size and chemical composition. As a second step, the adding-doubling method makes it possible to retrieve the total transmittance of the algal medium from the optical properties of the individual algal cells. The method was tested by comparing the simulated total transmittance spectra for dense marine microalgal cultures of Isochrysis galbana (small flagellates) and Phaeodactylum tricornutum (diatoms) to spectra measured using an experimental spectrophotometric setup. Our study revealed that the total transmittance spectra simulated for the quasi-spherical cells of Isochrysis galbana were in good agreement with the measured spectra over the whole spectral range. For Phaeodactylum tricornutum, large differences between simulated and measured spectra were observed over the blue part of the transmittance spectra, probably due to non-spherical shape of the algal cells. Prediction of the algal cell density, mean size and pigment composition from the total transmittance spectra measured on algal samples was also investigated using the reversal of the method. Mean cell size was successfully predicted for both species. The cell density was also successfully predicted for spherical Isochrysis galbana, with a relative error below 7%, but not for elongated Phaeodactylum tricornutum with a relative error up to 26%. The pigments total quantity and composition, the carotenoids:chlorophyll ratio in particular, were also successfully predicted for Isochrysis galbana with a relative error below 8%. However, the pigment predictions and measurements for Phaeodactylum tricornutum showed large discrepancies, with a relative error up to 88%. These results give strong support for the development of a promising tool providing rapid and accurate estimations of biomass and physiological status of a dense microalgal culture based on only light transmittance properties.
Subject(s)
Diatoms/chemistry , Haptophyta/chemistry , Microalgae/chemistry , Spectrophotometry/methods , Anisotropy , Cell Culture Techniques/instrumentation , Cell Culture Techniques/methods , Cell Shape , Cell Size , Computer Simulation , Diatoms/cytology , Diatoms/growth & development , Equipment Design , Haptophyta/cytology , Haptophyta/growth & development , Microalgae/cytology , Microalgae/growth & development , Models, Biological , Pigments, Biological/analysis , Spectrophotometry/instrumentationABSTRACT
The importance of heterotrophic bacteria relative to phytoplankton in the uptake of ammonium and nitrate was studied in Mediterranean coastal waters (Thau Lagoon) during autumn, when the Mediterranean Sea received the greatest allochthonous nutrient loads. Specific inhibitors and size-fractionation methods were used in combination with isotopic (15)N tracers. NO3 (-) and NH4 (+) uptake was dominated by phytoplankton (60 % on average) during the study period, which included a flood event. Despite lower biomass specific NH4 (+) and NO3 uptake rates, free-living heterotrophic bacteria contributed significantly (>30 %) to total microbial NH4 (+) and NO3 (-) uptake rates in low chlorophyll waters. Under these conditions, heterotrophic bacteria may be responsible for more than 50 % of primary production, using very little freshly produced phytoplankton exudates. In low chlorophyll coastal waters as reported during the present 3-month study, the heterotrophic bacteria seemed to depend to a greater extent on allochthonous N and C substrates than on autochthonous substrates derived from phytoplankton.
Subject(s)
Bacteria/metabolism , Nitrogen/metabolism , Seawater/microbiology , Bacteria/classification , Bacteria/genetics , Biomass , Mediterranean Region , Nitrogen/analysis , Phytoplankton/classification , Phytoplankton/metabolism , Seasons , Seawater/analysisABSTRACT
Dinoflagellate blooms are frequently observed under temporary eutrophication of coastal waters after heavy rains. Growth of these opportunistic microalgae is believed to be promoted by sudden input of nutrients and the absence or inefficiency of their natural enemies, such as grazers and parasites. Here, numerical simulations indicate that increasing nutrient availability not only promotes the formation of dinoflagellate blooms but can also stimulate their control by protozoan parasites. Moreover, high abundance of phytoplankton other than dinoflagellate hosts might have a significant dilution effect on the control of dinoflagellate blooms by parasites, either by resource competition with dinoflagellates (thus limiting the number of hosts available for infection) or by affecting numerical-functional responses of grazers that consume free-living parasite stages. These outcomes indicate that although both dinoflagellates and their protozoan parasites are directly affected by nutrient availability, the efficacy of the parasitic control of dinoflagellate blooms under temporary eutrophication depends strongly on the structure of the plankton community as a whole.
Subject(s)
Dinoflagellida/physiology , Dinoflagellida/parasitology , Food , Models, Biological , Parasites/physiology , Plankton/physiology , Animals , Computer Simulation , Eutrophication , Numerical Analysis, Computer-AssistedABSTRACT
The effects of grazing pressure and inorganic nutrient availability on the direct carbon transfer from freshly produced phytoplankton exudates to heterotrophic bacteria biomass production were studied in Mediterranean coastal waters. The short-term incorporation of ¹³C (H¹³CO3) in phytoplankton and bacterial lipid biomarkers was measured as well as the total bacterial carbon production (BP), viral lysis and the microbial community structure under three experimental conditions: (1) High inorganic Nutrient and High Grazing (HN + HG), (2) High inorganic Nutrient and Low Grazing (HN + LG) and (3) under natural in situ conditions with Low inorganic Nutrient and High Grazing (LN + HG) during spring. Under phytoplankton bloom conditions (HN + LG), the bacterial use of freshly produced phytoplankton exudates as a source of carbon, estimated from ¹³C enrichment of bacterial lipids, contributed more than half of the total bacterial production. However, under conditions of high grazing pressure on phytoplankton with or without the addition of inorganic nutrients (HN + HG and LN + HG), the ¹³C enrichment of bacterial lipids was low compared with the high total bacterial production. BP therefore seems to depend mainly on freshly produced phytoplankton exudates during the early phase of phytoplankton bloom period. However, BP seems mainly relying on recycled carbon from viral lysis and predators under high grazing pressure.
Subject(s)
Bacteria/metabolism , Carbon/metabolism , Heterotrophic Processes , Phytoplankton/growth & development , Seawater/microbiology , Biomass , Carbon Isotopes/analysis , Food Chain , France , Lipids/analysis , Mediterranean Sea , Phytoplankton/chemistry , Seasons , Seawater/chemistryABSTRACT
N2-fixing cyanobacteria represent a major source of new nitrogen and carbon for marine microbial communities, but little is known about their ecological interactions with associated microbiota. In this study we investigated the interactions between the unicellular N2-fixing cyanobacterium Cyanothece sp. Miami BG043511 and its associated free-living chemotrophic bacteria at different concentrations of nitrate and dissolved organic carbon and different temperatures. High temperature strongly stimulated the growth of Cyanothece, but had less effect on the growth and community composition of the chemotrophic bacteria. Conversely, nitrate and carbon addition did not significantly increase the abundance of Cyanothece, but strongly affected the abundance and species composition of the associated chemotrophic bacteria. In nitrate-free medium the associated bacterial community was co-dominated by the putative diazotroph Mesorhizobium and the putative aerobic anoxygenic phototroph Erythrobacter and after addition of organic carbon also by the Flavobacterium Muricauda. Addition of nitrate shifted the composition toward co-dominance by Erythrobacter and the Gammaproteobacterium Marinobacter. Our results indicate that Cyanothece modified the species composition of its associated bacteria through a combination of competition and facilitation. Furthermore, within the bacterial community, niche differentiation appeared to play an important role, contributing to the coexistence of a variety of different functional groups. An important implication of these findings is that changes in nitrogen and carbon availability due to, e.g., eutrophication and climate change are likely to have a major impact on the species composition of the bacterial community associated with N2-fixing cyanobacteria.
ABSTRACT
BACKGROUND: Small size eukaryotes play a fundamental role in the functioning of coastal ecosystems, however, the way in which these micro-organisms respond to combined effects of water temperature, UVB radiations (UVBR) and nutrient availability is still poorly investigated. RESULTS: We coupled molecular tools (18S rRNA gene sequencing and fingerprinting) with microscope-based identification and counting to experimentally investigate the short-term responses of small eukaryotes (<6 µm; from a coastal Mediterranean lagoon) to a warming treatment (+3°C) and UVB radiation increases (+20%) at two different nutrient levels. Interestingly, the increase in temperature resulted in higher pigmented eukaryotes abundances and in community structure changes clearly illustrated by molecular analyses. For most of the phylogenetic groups, some rearrangements occurred at the OTUs level even when their relative proportion (microscope counting) did not change significantly. Temperature explained almost 20% of the total variance of the small eukaryote community structure (while UVB explained only 8.4%). However, complex cumulative effects were detected. Some antagonistic or non additive effects were detected between temperature and nutrients, especially for Dinophyceae and Cryptophyceae. CONCLUSIONS: This multifactorial experiment highlights the potential impacts, over short time scales, of changing environmental factors on the structure of various functional groups like small primary producers, parasites and saprotrophs which, in response, can modify energy flow in the planktonic food webs.
Subject(s)
Biodiversity , Eukaryota/growth & development , Eukaryota/radiation effects , Ultraviolet Rays , DNA, Ribosomal/chemistry , DNA, Ribosomal/genetics , Eukaryota/cytology , Eukaryota/genetics , Mediterranean Region , Microscopy , Molecular Sequence Data , RNA, Ribosomal, 18S/genetics , Seawater/microbiology , Sequence Analysis, DNA , TemperatureABSTRACT
Association of microalgae culture and anaerobic digestion seems a promising technology for sustainable algal biomass and biogas production. The use of digestates for sustaining the growth of microalgae reduces the costs and the environmental impacts associated with the substantial algal nutrient requirements. A natural marine algae-bacteria consortium was selected by growing on a medium containing macro nutrients (ammonia, phosphate and acetate) specific of a digestate, and was submitted to a factorial experimental design with different levels of temperature, light and pH. The microalgal consortium reached a maximum C conversion efficiency (i.e. ratio between carbon content produced and carbon supplied through light photosynthetic C conversion and acetate) of 3.6%. The presence of bacteria increased this maximum C conversion efficiency up to 6.3%. The associated bacterial community was considered beneficial to the total biomass production by recycling the carbon lost during photosynthesis and assimilating organic by-products from anaerobic digestion.
Subject(s)
Bacteria, Anaerobic/physiology , Carbon/metabolism , Microalgae/physiology , Microbial Consortia/physiology , Photobioreactors/microbiology , Water Microbiology , Bacteria, Anaerobic/radiation effects , Cell Proliferation , Light , Microalgae/radiation effects , Microbial Consortia/radiation effects , Oceans and SeasABSTRACT
Positive relationships between heterotrophic bacteria and particulate phytoplankton production (respectively, BP and PPP) have been reported for several areas, suggesting that material produced by phytoplankton was a major substrate for bacterial growth. Since then, thousands of simultaneous measurements of both PPP and BP have been performed. A review of these data showed that BP may exceed PPP considerably (median ranged between 132% and 484%) in all aquatic systems with the lowest PPP. In oceanic waters, BP did not seem to be temporally synchronized with PPP and the median BP : PPP ratio is 15% with moderate PPP, but the immediate bacterial carbon (C) demand (including bacterial respiration) was greater than the corresponding total primary production (i.e. dissolved and particulate primary production) for >80% of both volumetric and areal datasets. In freshwaters, the strong covariation observed between BP and PPP seemed mainly due to a common response to sudden nutrient inputs into enclosed systems, leading to a similar range of production rates and temporal synchronicities. Indeed, phytoplankton exudates contributed directly to only 32% (median) of BP when C-tracking experiments were performed in freshwaters. Therefore, because direct C dependency of bacteria on phytoplankton is questionable, other C sources might be more significant for bacterial growth.