RESUMO
Cable bacteria embed a network of conductive protein fibers in their cell envelope that efficiently guides electron transport over distances spanning up to several centimeters. This form of long-distance electron transport is unique in biology and is mediated by a metalloprotein with a sulfur-coordinated nickel (Ni) cofactor. However, the molecular structure of this cofactor remains presently unknown. Here, we applied multi-wavelength Raman microscopy to identify cell compounds linked to the unique cable bacterium physiology, combined with stable isotope labeling, and orientation-dependent and ultralow-frequency Raman microscopy to gain insight into the structure and organization of this novel Ni-cofactor. Raman spectra of native cable bacterium filaments reveal vibrational modes originating from cytochromes, polyphosphate granules, proteins, as well as the Ni-cofactor. After selective extraction of the conductive fiber network from the cell envelope, the Raman spectrum becomes simpler, and primarily retains vibrational modes associated with the Ni-cofactor. These Ni-cofactor modes exhibit intense Raman scattering as well as a strong orientation-dependent response. The signal intensity is particularly elevated when the polarization of incident laser light is parallel to the direction of the conductive fibers. This orientation dependence allows to selectively identify the modes that are associated with the Ni-cofactor. We identified 13 such modes, some of which display strong Raman signals across the entire range of applied wavelengths (405-1,064 nm). Assignment of vibrational modes, supported by stable isotope labeling, suggest that the structure of the Ni-cofactor shares a resemblance with that of nickel bis(1,2-dithiolene) complexes. Overall, our results indicate that cable bacteria have evolved a unique cofactor structure that does not resemble any of the known Ni-cofactors in biology.
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Biogeochemical sulfur cycling in sulfidic karst systems is largely driven by abiotic and biological sulfide oxidation, but the fate of elemental sulfur (S0 ) that accumulates in these systems is not well understood. The Frasassi Cave system (Italy) is intersected by a sulfidic aquifer that mixes with small quantities of oxygen-rich meteoric water, creating Proterozoic-like conditions and supporting a prolific ecosystem driven by sulfur-based chemolithoautotrophy. To better understand the cycling of S0 in this environment, we examined the geochemistry and microbiology of sediments underlying widespread sulfide-oxidizing mats dominated by Beggiatoa. Sediment populations were dominated by uncultivated relatives of sulfur cycling chemolithoautotrophs related to Sulfurovum, Halothiobacillus, Thiofaba, Thiovirga, Thiobacillus, and Desulfocapsa, as well as diverse uncultivated anaerobic heterotrophs affiliated with Bacteroidota, Anaerolineaceae, Lentimicrobiaceae, and Prolixibacteraceae. Desulfocapsa and Sulfurovum populations accounted for 12%-26% of sediment 16S rRNA amplicon sequences and were closely related to isolates which carry out autotrophic S0 disproportionation in pure culture. Gibbs energy (∆Gr ) calculations revealed that S0 disproportionation under in situ conditions is energy yielding. Microsensor profiles through the mat-sediment interface showed that Beggiatoa mats consume dissolved sulfide and oxygen, but a net increase in acidity was only observed in the sediments below. Together, these findings suggest that disproportionation is an important sink for S0 generated by microbial sulfide oxidation in this oxygen-limited system and may contribute to the weathering of carbonate rocks and sediments in sulfur-rich environments.
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In Parkinson's disease, pathogenic factors such as the intraneuronal accumulation of the protein α-synuclein affect key metabolic processes. New approaches are required to understand how metabolic dysregulations cause degeneration of vulnerable subtypes of neurons in the brain. Here, we apply correlative electron microscopy and NanoSIMS isotopic imaging to map and quantify 13C enrichments in dopaminergic neurons at the subcellular level after pulse-chase administration of 13C-labeled glucose. To model a condition leading to neurodegeneration in Parkinson's disease, human α-synuclein was unilaterally overexpressed in the substantia nigra of one brain hemisphere in rats. When comparing neurons overexpressing α-synuclein to those located in the control hemisphere, the carbon anabolism and turnover rates revealed metabolic anomalies in specific neuronal compartments and organelles. Overexpression of α-synuclein enhanced the overall carbon turnover in nigral neurons, despite a lower relative incorporation of carbon inside the nucleus. Furthermore, mitochondria and Golgi apparatus showed metabolic defects consistent with the effects of α-synuclein on inter-organellar communication. By revealing changes in the kinetics of carbon anabolism and turnover at the subcellular level, this approach can be used to explore how neurodegeneration unfolds in specific subpopulations of neurons.
Assuntos
Doença de Parkinson , alfa-Sinucleína , Ratos , Humanos , Animais , alfa-Sinucleína/metabolismo , Doença de Parkinson/patologia , Marcação por Isótopo , Neurônios Dopaminérgicos/metabolismo , Encéfalo/patologia , Substância Negra/metabolismoRESUMO
Ocean plastic pollution is a severe environmental problem but most of the plastic that has been released to the ocean since the 1950s is unaccounted for. Although fungal degradation of marine plastics has been suggested as a potential sink mechanism, unambiguous proof of plastic degradation by marine fungi, or other microbes, is scarce. Here we applied stable isotope tracing assays with 13C-labeled polyethylene to measure biodegradation rates and to trace the incorporation of plastic-derived carbon into individual cells of the yeast Rhodotorula mucilaginosa, which we isolated from the marine environment. 13C accumulation in the CO2 pool during 5-day incubation experiments with R. mucilaginosa and UV-irradiated 13C-labeled polyethylene as a sole energy and carbon source translated to degradation rates of 3.8% yr-1 of the initially added substrate. Furthermore, nanoSIMS measurements revealed substantial incorporation of polyethylene-derived carbon into fungal biomass. Our results demonstrate the potential of R. mucilaginosa to mineralize and assimilate carbon from plastics and suggest that fungal plastic degradation may be an important sink for polyethylene litter in the marine environment.
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So far, only members of the bacterial phyla Proteobacteria and Verrucomicrobia are known to grow methanotrophically under aerobic conditions. Here we report that this metabolic trait is also observed within the Actinobacteria. We enriched and cultivated a methanotrophic Mycobacterium from an extremely acidic biofilm growing on a cave wall at a gaseous chemocline interface between volcanic gases and the Earth's atmosphere. This Mycobacterium, for which we propose the name Candidatus Mycobacterium methanotrophicum, is closely related to well-known obligate pathogens such as M. tuberculosis and M. leprae. Genomic and proteomic analyses revealed that Candidatus M. methanotrophicum expresses a full suite of enzymes required for aerobic growth on methane, including a soluble methane monooxygenase that catalyses the hydroxylation of methane to methanol and enzymes involved in formaldehyde fixation via the ribulose monophosphate pathway. Growth experiments combined with stable isotope probing using 13C-labelled methane confirmed that Candidatus M. methanotrophicum can grow on methane as a sole carbon and energy source. A broader survey based on 16S metabarcoding suggests that species closely related to Candidatus M. methanotrophicum may be abundant in low-pH, high-methane environments.
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Ecossistema , Mycobacterium , Proteômica , Filogenia , Metano/metabolismo , Mycobacterium/genéticaRESUMO
Cable bacteria are multicellular sulfide oxidizing bacteria that display a unique metabolism based on long-distance electron transport. Cells in deeper sediment layers perform the sulfide oxidizing half-reaction whereas cells in the surface layers of the sediment perform the oxygen-reducing half-reaction. These half-reactions are coupled via electron transport through a conductive fiber network that runs along the shared cell envelope. Remarkably, only the sulfide oxidizing half-reaction is coupled to biosynthesis and growth whereas the oxygen reducing half-reaction serves to rapidly remove electrons from the conductive fiber network and is not coupled to energy generation and growth. Cells residing in the oxic zone are believed to (temporarily) rely on storage compounds of which polyphosphate (poly-P) is prominently present in cable bacteria. Here we investigate the role of poly-P in the metabolism of cable bacteria within the different redox environments. To this end, we combined nanoscale secondary ion mass spectrometry with dual-stable isotope probing (13C-DIC and 18O-H2O) to visualize the relationship between growth in the cytoplasm (13C-enrichment) and poly-P activity (18O-enrichment). We found that poly-P was synthesized in almost all cells, as indicated by 18O enrichment of poly-P granules. Hence, poly-P must have an important function in the metabolism of cable bacteria. Within the oxic zone of the sediment, where little growth is observed, 18O enrichment in poly-P granules was significantly lower than in the suboxic zone. Thus, both growth and poly-P metabolism appear to be correlated to the redox environment. However, the poly-P metabolism is not coupled to growth in cable bacteria, as many filaments from the suboxic zone showed poly-P activity but did not grow. We hypothesize that within the oxic zone, poly-P is used to protect the cells against oxidative stress and/or as a resource to support motility, while within the suboxic zone, poly-P is involved in the metabolic regulation before cells enter a non-growing stage.
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Stable isotope probing (SIP) combined with nano-scale secondary ion mass spectrometry (nanoSIMS) is a powerful approach to quantify assimilation rates of elements such as C and N into individual microbial cells. Here, we use mathematical modeling to investigate how the derived rate estimates depend on the model used to describe substrate assimilation by a cell during a SIP incubation. We show that the most commonly used model, which is based on the simplifying assumptions of linearly increasing biomass of individual cells over time and no cell division, can yield underestimated assimilation rates when compared to rates derived from a model that accounts for cell division. This difference occurs because the isotopic labeling of a dividing cell increases more rapidly over time compared to a non-dividing cell and becomes more pronounced as the labeling increases above a threshold value that depends on the cell cycle stage of the measured cell. Based on the modeling results, we present formulae for estimating assimilation rates in cells and discuss their underlying assumptions, conditions of applicability, and implications for the interpretation of intercellular variability in assimilation rates derived from nanoSIMS data, including the impacts of storage inclusion metabolism. We offer the formulae as a Matlab script to facilitate rapid data evaluation by nanoSIMS users.
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Filamentous cable bacteria display long-range electron transport, generating electrical currents over centimeter distances through a highly ordered network of fibers embedded in their cell envelope. The conductivity of these periplasmic wires is exceptionally high for a biological material, but their chemical structure and underlying electron transport mechanism remain unresolved. Here, we combine high-resolution microscopy, spectroscopy, and chemical imaging on individual cable bacterium filaments to demonstrate that the periplasmic wires consist of a conductive protein core surrounded by an insulating protein shell layer. The core proteins contain a sulfur-ligated nickel cofactor, and conductivity decreases when nickel is oxidized or selectively removed. The involvement of nickel as the active metal in biological conduction is remarkable, and suggests a hitherto unknown form of electron transport that enables efficient conduction in centimeter-long protein structures.
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Proteínas de Bactérias/química , Deltaproteobacteria/metabolismo , Condutividade Elétrica , Transporte de Elétrons/fisiologia , Níquel/química , EletricidadeRESUMO
Marine diazotrophs are a diverse group with key roles in biogeochemical fluxes linked to primary productivity. The unicellular, diazotrophic cyanobacterium Cyanothece is widely found in coastal, subtropical oceans. We analyze the consequences of diazotrophy on growth efficiency, compared to NO3 --supported growth in Cyanothece, to understand how cells cope with N2-fixation when they also have to face carbon limitation, which may transiently affect populations in coastal environments or during blooms of phytoplankton communities. When grown in obligate diazotrophy, cells face the double burden of a more ATP-demanding N-acquisition mode and additional metabolic losses imposed by the transient storage of reducing potential as carbohydrate, compared to a hypothetical N2 assimilation directly driven by photosynthetic electron transport. Further, this energetic burden imposed by N2-fixation could not be alleviated, despite the high irradiance level within the cultures, because photosynthesis was limited by the availability of dissolved inorganic carbon (DIC), and possibly by a constrained capacity for carbon storage. DIC limitation exacerbates the costs on growth imposed by nitrogen fixation. Therefore, the competitive efficiency of diazotrophs could be hindered in areas with insufficient renewal of dissolved gases and/or with intense phytoplankton biomass that both decrease available light energy and draw the DIC level down.
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Cable bacteria are multicellular, Gram-negative filamentous bacteria that display a unique division of metabolic labor between cells. Cells in deeper sediment layers are oxidizing sulfide, while cells in the surface layers of the sediment are reducing oxygen. The electrical coupling of these two redox half reactions is ensured via long-distance electron transport through a network of conductive fibers that run in the shared cell envelope of the centimeter-long filament. Here we investigate how this unique electrogenic metabolism is linked to filament growth and cell division. Combining dual-label stable isotope probing (13C and 15N), nanoscale secondary ion mass spectrometry, fluorescence microscopy and genome analysis, we find that the cell cycle of cable bacteria cells is highly comparable to that of other, single-celled Gram-negative bacteria. However, the timing of cell growth and division appears to be tightly and uniquely controlled by long-distance electron transport, as cell division within an individual filament shows a remarkable synchronicity that extends over a millimeter length scale. To explain this, we propose the "oxygen pacemaker" model in which a filament only grows when performing long-distance transport, and the latter is only possible when a filament has access to oxygen so it can discharge electrons from its internal electrical network.
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Unicellular nitrogen fixing cyanobacteria (UCYN) are abundant members of phytoplankton communities in a wide range of marine environments, including those with rapidly changing nitrogen (N) concentrations. We hypothesized that differences in N availability (N2 vs. combined N) would cause UCYN to shift strategies of intracellular N and C allocation. We used transmission electron microscopy and nanoscale secondary ion mass spectrometry imaging to track assimilation and intracellular allocation of 13C-labeled CO2 and 15N-labeled N2 or NO3 at different periods across a diel cycle in Cyanothece sp. ATCC 51142. We present new ideas on interpreting these imaging data, including the influences of pre-incubation cellular C and N contents and turnover rates of inclusion bodies. Within cultures growing diazotrophically, distinct subpopulations were detected that fixed N2 at night or in the morning. Additional significant within-population heterogeneity was likely caused by differences in the relative amounts of N assimilated into cyanophycin from sources external and internal to the cells. Whether growing on N2 or NO3, cells prioritized cyanophycin synthesis when N assimilation rates were highest. N assimilation in cells growing on NO3 switched from cyanophycin synthesis to protein synthesis, suggesting that once a cyanophycin quota is met, it is bypassed in favor of protein synthesis. Growth on NO3 also revealed that at night, there is a very low level of CO2 assimilation into polysaccharides simultaneous with their catabolism for protein synthesis. This study revealed multiple, detailed mechanisms underlying C and N management in Cyanothece that facilitate its success in dynamic aquatic environments.
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Cyanobacterial mats were hotspots of biogeochemical cycling during the Precambrian. However, mechanisms that controlled O2 release by these ecosystems are poorly understood. In an analog to Proterozoic coastal ecosystems, the Frasassi sulfidic springs mats, we studied the regulation of oxygenic and sulfide-driven anoxygenic photosynthesis (OP and AP) in versatile cyanobacteria, and interactions with sulfur reducing bacteria (SRB). Using microsensors and stable isotope probing we found that dissolved organic carbon (DOC) released by OP fuels sulfide production, likely by a specialized SRB population. Increased sulfide fluxes were only stimulated after the cyanobacteria switched from AP to OP. O2 production triggered migration of large sulfur-oxidizing bacteria from the surface to underneath the cyanobacterial layer. The resultant sulfide shield tempered AP and allowed OP to occur for a longer duration over a diel cycle. The lack of cyanobacterial DOC supply to SRB during AP therefore maximized O2 export. This mechanism is unique to benthic ecosystems because transitions between metabolisms occur on the same time scale as solute transport to functionally distinct layers, with the rearrangement of the system by migration of microorganisms exaggerating the effect. Overall, cyanobacterial versatility disrupts the synergistic relationship between sulfide production and AP, and thus enhances diel O2 production.
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Cianobactérias , Ecossistema , Oxigênio , Fotossíntese , SulfetosRESUMO
Analytical capabilities of Nanoscopic Secondary Ion Mass Spectrometry (nano-SIMS) and Synchrotron Radiation based X-ray Fluorescence (SR nano-XRF) techniques were compared for nanochemical imaging of polymorphonuclear human neutrophils (PMNs). PMNs were high pressure frozen (HPF), cryo-substituted, embedded in Spurr's resin and cut in thin sections (500 nm and 2 µm for both techniques resp.) Nano-SIMS enabled nanoscale mapping of isotopes of C, N, O, P and S, while SR based nano-XRF enabled trace level imaging of metals like Ca, Mn, Fe, Ni, Cu and Zn at a resolution of approx. 50 nm. The obtained elemental distributions were compared with those of whole, cryofrozen PMNs measured at the newly developed ID16A nano-imaging beamline at the European Synchrotron Radiation Facility (ESRF) in Grenoble, France. Similarities were observed for elements more tightly bound to the cell structure such as phosphorus and sulphur, while differences for mobile ions such as chlorine and potassium were more pronounced. Due to the observed elemental redistribution of mobile ions such as potassium and chlorine, elemental analysis of high pressure frozen (HPF), cryo-substituted and imbedded cells should be interpreted critically. Although decreasing analytical sensitivity occurs due to the presence of ice, analysis of cryofrozen cells - close to their native state - remains the golden standard. In general, we found nanoscale secondary ion mass spectrometry (nano-SIMS) and synchrotron radiation based nanoscopic X-ray fluorescence (SR nano-XRF) to be two supplementary alternatives for nanochemical imaging of single cells at the nanoscale.
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Neutrófilos/citologia , Imagem Óptica , Análise de Célula Única , Espectrometria de Massa de Íon Secundário , Síncrotrons , Humanos , Tamanho da Partícula , Espectrometria por Raios X , Propriedades de SuperfícieRESUMO
Multicellularity is a key evolutionary innovation, leading to coordinated activity and resource sharing among cells, which generally occurs via the physical exchange of chemical compounds. However, filamentous cable bacteria display a unique metabolism in which redox transformations in distant cells are coupled via long-distance electron transport rather than an exchange of chemicals. This challenges our understanding of organismal functioning, as the link among electron transfer, metabolism, energy conservation, and filament growth in cable bacteria remains enigmatic. Here, we show that cells within individual filaments of cable bacteria display a remarkable dichotomy in biosynthesis that coincides with redox zonation. Nanoscale secondary ion mass spectrometry combined with 13C (bicarbonate and propionate) and 15N-ammonia isotope labeling reveals that cells performing sulfide oxidation in deeper anoxic horizons have a high assimilation rate, whereas cells performing oxygen reduction in the oxic zone show very little or no label uptake. Accordingly, oxygen reduction appears to merely function as a mechanism to quickly dispense of electrons with little to no energy conservation, while biosynthesis and growth are restricted to sulfide-respiring cells. Still, cells can immediately switch roles when redox conditions change, and show no differentiation, which suggests that the "community service" performed by the cells in the oxic zone is only temporary. Overall, our data reveal a division of labor and electrical cooperation among cells that has not been seen previously in multicellular organisms.
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Deltaproteobacteria/crescimento & desenvolvimento , Deltaproteobacteria/metabolismo , Eletricidade , Transporte de Elétrons , Amônia/metabolismo , Isótopos de Carbono , Espectrometria de Massa de Íon Secundário , Sulfetos/metabolismoRESUMO
At an altitude of 3,570 m, the volcanic lake Socompa in the Argentinean Andes is presently the highest site where actively forming stromatolite-like structures have been reported. Interestingly, pigment and microsensor analyses performed through the different layers of the stromatolites (50 mm-deep) showed steep vertical gradients of light and oxygen, hydrogen sulfide and pH in the porewater. Given the relatively good characterization of these physico-chemical gradients, the aim of this follow-up work was to specifically address how the bacterial diversity stratified along the top six layers of the stromatolites which seems the most metabolically important and diversified zone of the whole microbial community. We herein discussed how, in only 7 mm, a drastic succession of metabolic adaptations occurred: i.e., microbial communities shift from a UV-high/oxic world to an IR-low/anoxic/high H2S environment which force stratification and metabolic specialization of the bacterial community, thus, modulating the chemical faces of the Socompa stromatolites. The oxic zone was dominated by Deinococcus sp. at top surface (0.3 mm), followed by a second layer of Coleofasciculus sp. (0.3 to â¼2 mm). Sequences from anoxygenic phototrophic Alphaproteobacteria, along with an increasing diversity of phyla including Bacteroidetes, Spirochaetes were found at middle layers 3 and 4. Deeper layers (5-7 mm) were mostly occupied by sulfate reducers of Deltaproteobacteria, Bacteroidetes and Firmicutes, next to a high diversity and equitable community of rare, unclassified and candidate phyla. This analysis showed how microbial communities stratified in a physicochemical vertical profile and according to the light source. It also gives an insight of which bacterial metabolic capabilities might operate and produce a microbial cooperative strategy to thrive in one of the most extreme environments on Earth.
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We used microsensors to study the regulation of anoxygenic and oxygenic photosynthesis (AP and OP, respectively) by light and sulfide in a cyanobacterium dominating microbial mats from cold sulfidic springs. Both photosynthetic modes were performed simultaneously over all H2S concentrations (1-2200 µM) and irradiances (4-52 µmol photons m-2 s-1) tested. AP increased with H2S concentration while the sum of oxygenic and anoxygenic photosynthetic rates was constant at each light intensity. Thus, the total photosynthetically driven electron transport rate was solely controlled by the irradiance level. The partitioning between the rates of these two photosynthetic modes was regulated by both light and H2S concentration. The plastoquinone pool (PQ) receives electrons from sulfide:quinone:reductase (SQR) in AP and from photosystem II (PSII) in OP. It is thus the link in the electron transport chain where both pathways intersect, and the compound that controls their partitioning. We fitted our data with a model of the photosynthetic electron transport that includes the kinetics of plastoquinone reduction and oxidation. The model results confirmed that the observed partitioning between photosynthetic modes can be explained by a simple kinetic control based on the affinity of SQR and PSII toward PQ. The SQR enzyme and PSII have similar affinities toward PQ, which explains the concurrent OP and AP over an astonishingly wide range of H2S concentrations and irradiances. The elegant kinetic control of activity makes the cyanobacterium successful in the fluctuating spring environment. We discuss how these specific regulation mechanisms may have played a role in ancient H2S-rich oceans.
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Phosphorus is an essential nutrient for life. The release of phosphorus from sediments is critical in sustaining phytoplankton growth in many aquatic systems and is pivotal to eutrophication and the development of bottom water hypoxia. Conventionally, sediment phosphorus release is thought to be controlled by changes in iron oxide reduction driven by variations in external environmental factors, such as organic matter input and bottom water oxygen. Here, we show that internal shifts in microbial communities, and specifically the population dynamics of cable bacteria, can also induce strong seasonality in sedimentary iron-phosphorus dynamics. Field observations in a seasonally hypoxic coastal basin demonstrate that the long-range electrogenic metabolism of cable bacteria leads to a dissolution of iron sulfides in winter and spring. Subsequent oxidation of the mobilized ferrous iron with manganese oxides results in a large stock of iron-oxide-bound phosphorus below the oxic zone. In summer, when bottom water hypoxia develops and cable bacteria are undetectable, the phosphorus associated with these iron oxides is released, strongly increasing phosphorus availability in the water column. Future research should elucidate whether formation of iron-oxide-bound phosphorus driven by cable bacteria, as observed in this study, contributes to the seasonality in iron-phosphorus cycling in aquatic sediments worldwide.
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Bactérias/metabolismo , Sedimentos Geológicos/química , Sedimentos Geológicos/microbiologia , Ferro/metabolismo , Fósforo/metabolismo , Eutrofização , Compostos Férricos/química , Compostos Férricos/metabolismo , Compostos Ferrosos/química , Compostos Ferrosos/metabolismo , Ferro/análise , Países Baixos , Oxirredução , Oxigênio/metabolismo , Fósforo/análise , Dinâmica Populacional , Estações do Ano , Água/químicaRESUMO
Recent coral optics studies have revealed the presence of steep light gradients and optical microniches in tissues of symbiont-bearing corals. Yet, it is unknown whether such resource stratification allows for physiological differences of Symbiodinium within coral tissues. Using a combination of stable isotope labelling and nanoscale secondary ion mass spectrometry, we investigated in hospite carbon fixation of individual Symbiodinium as a function of the local O2 and light microenvironment within the coral host determined with microsensors. We found that net carbon fixation rates of individual Symbiodinium cells differed on average about sixfold between upper and lower tissue layers of single coral polyps, whereas the light and O2 microenvironments differed ~15- and 2.5-fold, respectively, indicating differences in light utilisation efficiency along the light microgradient within the coral tissue. Our study suggests that the structure of coral tissues might be conceptually similar to photosynthetic biofilms, where steep physico-chemical gradients define form and function of the local microbial community.
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Antozoários/parasitologia , Carbono/metabolismo , Dinoflagellida/fisiologia , Simbiose , Animais , Antozoários/fisiologia , Antozoários/efeitos da radiação , Ciclo do Carbono , Dinoflagellida/efeitos da radiação , Luz , Fotossíntese/efeitos da radiaçãoRESUMO
We studied the interaction between phototrophic and chemolithoautotrophic sulphide-oxidizing microorganisms in natural microbial mats forming in sulphidic streams. The structure of these mats varied between two end-members: one characterized by a layer dominated by large sulphur-oxidizing bacteria (SOB; mostly Beggiatoa-like) on top of a cyanobacterial layer (B/C mats) and the other with an inverted structure (C/B mats). C/B mats formed where the availability of oxygen from the water column was limited (<5 µm). Aerobic chemolithotrophic activity of the SOB depended entirely on oxygen produced locally by cyanobacteria during high light conditions. In contrast, B/C mats formed at locations where oxygen in the water column was comparatively abundant (>45 µM) and continuously present. Here SOB were independent of the photosynthetic activity of cyanobacteria and outcompeted the cyanobacteria in the uppermost layer of the mat where energy sources for both functional groups were concentrated. Outcompetition of photosynthetic microbes in the presence of light was facilitated by the decoupling of aerobic chemolithotrophy and oxygenic phototrophy. Remarkably, the B/C mats conserved much less energy than the C/B mats, although similar amounts of light and chemical energy were available. Thus ecosystems do not necessarily develop towards optimal energy usage. Our data suggest that, when two independent sources of energy are available, the structure and activity of microbial communities is primarily determined by the continuous rather than the intermittent energy source, even if the time-integrated energy flux of the intermittent energy source is greater.
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Beggiatoa/fisiologia , Cianobactérias/fisiologia , Consórcios Microbianos , Oxigênio/química , Fotossíntese , Sulfetos/química , Carbono , Concentração de Íons de Hidrogênio , Luz , Microscopia , Processos Fototróficos , Água/químicaRESUMO
We used hyperspectral imaging to study short-term effects of bioturbation by lugworms (Arenicola marina) on the surficial biomass of microphytobenthos (MPB) in permeable marine sediments. Within days to weeks after the addition of a lugworm to a homogenized and recomposed sediment, the average surficial MPB biomass and its spatial heterogeneity were, respectively, 150-250% and 280% higher than in sediments without lugworms. The surficial sediment area impacted by a single medium-sized lugworm (~4 g wet weight) over this time-scale was at least 340 cm2. While sediment reworking was the primary cause of the increased spatial heterogeneity, experiments with lugworm-mimics together with modeling showed that bioadvective porewater transport from depth to the sediment surface, as induced by the lugworm ventilating its burrow, was the main cause of the increased surficial MPB biomass. Although direct measurements of nutrient fluxes are lacking, our present data show that enhanced advective supply of nutrients from deeper sediment layers induced by faunal ventilation is an important mechanism that fuels high primary productivity at the surface of permeable sediments even though these systems are generally characterized by low standing stocks of nutrients and organic material.