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In aquatic environments, the consensus of viral impact on bacterial carbon metabolism with the nutrient environment as an important axis is limited. Henceforth, we explored the viral regulation of carbon-based bacterial growth efficiency (BGE) in a set of freshwater systems from French Massif Central, which were broadly classified based on two trophic statuses: eutrophic and non-eutrophic lakes. Comparative analysis showed that microbial abundances (viruses and bacteria) were 3-fold higher in eutrophic compared with non-eutrophic lakes, and so were bacterial production and viral lytic infection. The observed variability in BGE (10-60%) was explained by the uncoupling between bacterial respiration and production. Viruses through selective lysis of susceptible host communities had an antagonistic impact on BGE in the eutrophic lakes, whereas the release of substrates via viral shunt exerted a synergistic influence on the carbon metabolism of non-targeted host populations in non-eutrophic lakes. The decisive effect of the two individual processes (i.e., lysis and substrate release) on BGE was supported by regressions of bacterial abundance as a function of bacterial production, which is considered as a proxy of top-down processes. The role of viruses through their negative impact via mortality and positive impact via substrate supply can eventually have implications on carbon transfer through bacterioplankton in freshwaters.

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In freshwater environments, limited data exist on the impact of mortality forces (viruses and heterotrophic nanoflagellates) on bacterial growth efficiency (BGE, index of bacterial carbon metabolism) compared to resource availability. An investigation to determine the relative influence of viral lysis and flagellate predation (top-down forces) on BGE was conducted in a mesotrophic freshwater system (Lake Goule, France) with time and space. Viral abundance was significantly (p < 0.001) related to bacterial abundance by a power law function with an exponent less than 1, emphasizing that the increases in host population (bacteria) together with viruses were not proportionate. A lytic viral strategy was evident throughout the study period, with high lysis of the bacterial population (up to 60%) supported by viral production rates. Viral processes (lysis and production) that were influenced by bacterial production and heterotrophic nanoflagellate abundance had a positive impact on BGE. Estimates of BGE were variable (9.9−45.5%) due to uncoupling between two metabolic parameters­namely bacterial production and respiration. The existence of a synergistic relationship between viruses and flagellates with bacteria in Lake Goule highlighted the decisive impact of top-down agents in sustaining the bacterial carbon metabolism of non-infected population through the nature of vital resources released via mortality processes.

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Accurate estimates of bacterial carbon metabolic rates are indispensable for understanding the regulation of carbon fluxes in aquatic environments. Here, changes in bacterial growth, production, and cell volume in both pre-filtered and unfiltered seawater during 24 h incubation were monitored. The methodological artifacts during Winkler bacterial respiration (BR) measurements in subtropical Hong Kong coastal waters were assessed. Bacterial abundance increased by 3- and 1.8-fold in the pre-filtered and unfiltered seawater after incubation, respectively. Bacterial production (BP) and cell volume also showed significant enhancement. Compared with the BR measurements obtained by the Winkler method, the instantaneous free-living BR measurements, after correction, decreased by ~ 70%. The time-integrated free-living BR and BP during 24 h incubation in the pre-filtered sample provided an improved estimate of bacterial growth efficiency, which increased by ~ 52% compared to the common estimations using the noncomparable measurements of integrated free-living BR and instantaneous total BP. The overestimation of BR also exaggerated the contribution of bacteria to community respiration, affecting the understanding on the metabolic state of the marine ecosystems. Furthermore, the BR estimates by the Winkler method may be more biased in environments with a higher bacterial growth rate and tightly coupled grazing mortality, as well as in those with higher nutrient concentrations. These results reveal obvious problems associated with the BR methodology and raise a warning for caution when comparing BP and BR, as well as when making estimations of carbon flow through the complex microbial networks in aquatic ecosystems. Supplementary Information: The online version contains supplementary material available at 10.1007/s42995-022-00133-2.

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Global warming scenarios indicate that in subarctic regions, the precipitation will increase in the future. Coastal bacteria will thus receive increasing organic carbon sources from land runoff. How such changes will affect the function and taxonomic composition of coastal bacteria is poorly known. We performed a 10-day experiment with two isolated bacteria: Shewanella baltica from a seaside location and Duganella sp. from a river mouth, and provided them with a plankton and a river extract as food substrate. The bacterial growth and carbon consumption were monitored over the experimental period. Shewanella and Duganella consumed 40% and 30% of the plankton extract, respectively, while the consumption of the river extract was low for both bacteria, ∼1%. Shewanella showed the highest bacterial growth efficiency (BGE) (12%) when grown on plankton extract, while when grown on river extract, the BGE was only 1%. Duganella showed low BGE when grown on plankton extract (< 1%) and slightly higher BGE when grown on river extract (2%). The cell growth yield of Duganella was higher than that of Shewanella when grown on river extract. These results indicate that Duganella is more adapted to terrestrial organic substrates with low nutritional availability, while Shewanella is adapted to eutrophied conditions. The different growth performance of the bacteria could be traced to genomic variations. A closely related genome of Shewanella was shown to harbor genes for the sequestration of autochthonously produced carbon substrates, while Duganella contained genes for the degradation of relatively refractive terrestrial organic matter. The results may reflect the influence of environmental drivers on bacterial community composition in natural aquatic environments. Elevated inflows of terrestrial organic matter to coastal areas in subarctic regions would lead to increased occurrence of bacteria adapted to the degradation of complex terrestrial compounds with a low bioavailability.

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The bioavailability of organic matter (OM) to marine heterotrophic bacterioplankton is determined by both the chemical composition of OM and the microbial community composition. In the current study, changes in OM bioavailability were identified at Ocean Station Papa as part of the 2018 Export Processes in the Ocean from Remote Sensing (EXPORTS) field study. Removal rates of carbon (C) in controlled experiments were significantly correlated with the initial composition of total hydrolyzable amino acids, and C removal rates were high when the amino acid degradation index suggested a more labile composition. Carbon remineralization rates averaged 0.19 ± 0.08 µmol C L-1 d-1 over 6-10 days while bacterial growth efficiencies averaged 31 ± 7%. Amino acid composition and tandem mass spectrometry analysis of compound classes also revealed transformations to a more degraded OM composition during experiments. There was a log2-fold increase in the relative abundances of 16S rDNA-resolved bacterioplankton taxa in most experiments by members of the Methylophilaceae family (OM43 genus) and KI89A order. Additionally, when OM was more bioavailable, relative abundances increased by at least threefold for the classes Bacteroidetes (Flavobacteriaceae NS2b genus), Alphaproteobacteria (Rhodobacteraceae Sulfitobacter genus), and Gammaproteobacteria (Alteromonadales and Ectothiorhodospiraceae orders). Our data suggest that a diverse group of bacterioplankton was responsible for removing organic carbon and altering the OM composition to a more degraded state. Elevated community diversity, as inferred from the Shannon-Wiener H index, may have contributed to relatively high growth efficiencies by the bacterioplankton. The data presented here shed light on the interconnections between OM bioavailability and key bacterioplankton taxa for the degradation of marine OM.

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Growth energetics and metabolic efficiency contribute to the lifestyle and habitat imprint of microorganisms. Roseobacters constitute one of the most abundant and successful marine bacterioplankton groups. Here, we reflect on the energetics and metabolic efficiency of Phaeobacter inhibens DSM 17395, a versatile heterotrophic roseobacter. Fourteen different substrates (five sugars and nine amino acids) and their degradation pathways were assessed for energetic efficiencies based on catabolic ATP yields, calculated from net formed ATP and reducing equivalents. The latter were converted into ATP by employing the most divergent coupling ratios (i.e., ions per ATP) currently known for F1Fo ATP synthases in heterotrophic bacteria. The catabolic ATP yields of the pathways studied in P. inhibens differed ∼3-fold. The actual free energy costs for ATP synthesis were estimated at 81.6 kJ per mol ATP (3.3 ions per ATP) or 104.2 kJ per mol ATP (4.3 ions per ATP), yielding an average thermodynamic efficiency of ∼37.7% or ∼29.5%, respectively. Growth performance (rates, yields) and carbon assimilation efficiency were determined for P. inhibens growing in process-controlled bioreactors with 10 different single substrates (Glc, Man, N-acetylglucosamine [Nag], Phe, Trp, His, Lys, Thr, Val, or Leu) and with 2 defined substrate mixtures. The efficiencies of carbon assimilation into biomass ranged from ∼28% to 61%, with His/Trp and Thr/Leu yielding the lowest and highest levels. These efficiencies correlated with catabolic and ATP yields only to some extent. Substrate-specific metabolic demands and/or functions, as well as the compositions of the substrate mixtures, apparently affected the energetic costs of growth. These include energetic burdens associated with, e.g., slow growth, stress, and/or the production of tropodithietic acid.IMPORTANCE Heterotrophic members of the bacterioplankton serve the marine ecosystem by transforming organic matter, an activity that is governed by the bacterial growth efficiencies (BGEs) obtained under given environmental conditions. In marine ecology, the concept of BGE refers to the carbon assimilation efficiency within natural communities. The marine bacterium studied here, Phaeobacter inhibens DSM 17395, is a copiotrophic representative of the globally abundant Roseobacter group, and the 15 catabolic pathways investigated are widespread among these marine heterotrophs. Combining pathway-specific catabolic ATP yields with in-depth quantitative physiological data could (i) provide a new baseline for the study of growth energetics and efficiency in further Roseobacter group members and other copiotrophic marine bacteria in productive coastal ecosystems and (ii) contribute to a better understanding of the factors controlling BGE (including the additional energetic burden arising from widespread secondary-metabolite formation) based on laboratory studies with pure cultures.

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Bacterial production (BP), respiration (BR) and growth efficiency (BGE) were simultaneously determined along an environmental gradient in the Pearl River Estuary (PRE) in the wet season (May 2015) and the dry season (January 2016), in order to examine bacterial responses to the riverine dissolved organic carbon (DOC) in the PRE. The Pearl River discharge delivered labile dissolved organic matters (DOM) with low DOC:DON ratio, resulting in a clear gradient in DOC concentrations and DOC:DON ratios. BP (3.93-144 µg C L-1 d-1) was more variable than BR (64.6-567 µg C L-1 d-1) in terms of the percentage, along an environmental gradient in the PRE. In response to riverine DOC input, BP and the cell-specific BP increased; in contrast, the cell-specific bacterial respiration declined, likely because labile riverine DOC mitigated energetic cost for cell maintenance. Consequently, an increase in bacterial respiration was less than expected. Our findings implied that the input of highly bioavailable riverine DOC altered the carbon portioning between anabolic and catabolic pathways, consequently decreasing the fraction of DOC that bacterioplankton utilized for bacterial respiration. This might be one of the underlying mechanisms for the low CO2 degassing in the PRE receiving large amounts of sewage DOC.

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Increases of atmospheric CO2 concentrations due to human activity and associated effects on aquatic ecosystems are recognized as an environmental issue at a global scale. Growing attention is being paid to CO2 enrichment effects under multiple stresses or fluctuating environmental conditions in order to extrapolate from laboratory-scale experiments to natural systems. We carried out a mesocosm experiment in coastal water with an assemblage of three model phytoplankton species and their associated bacteria under the influence of elevated CO2 concentrations. Net community production and the metabolic characteristics of the phytoplankton and bacteria were monitored to elucidate how these organisms responded to CO2 enrichment during the course of the algal bloom. We found that CO2 enrichment (1000µatm) significantly enhanced gross primary production and the ratio of photosynthesis to chlorophyll a by approximately 38% and 39%, respectively, during the early stationary phase of the algal bloom. Although there were few effects on bulk bacterial production, a significant decrease of bulk bacterial respiration (up to 31%) at elevated CO2 resulted in an increase of bacterial growth efficiency. The implication is that an elevation of CO2 concentrations leads to a reduction of bacterial carbon demand and enhances carbon transfer efficiency through the microbial loop, with a greater proportion of fixed carbon being allocated to bacterial biomass and less being lost as CO2. The contemporaneous responses of phytoplankton and bacterial metabolism to CO2 enrichment increased net community production by about 45%, an increase that would have profound implications for the carbon cycle in coastal marine ecosystems.

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The impact of solar radiation on dissolved organic matter (DOM) derived from 3 different sources (seawater, eelgrass leaves and river water) and the effect on the bacterial carbon cycling and diversity were investigated. Seawater with DOM from the sources was first either kept in the dark or exposed to sunlight (4 days), after which a bacterial inoculum was added and incubated for 4 additional days. Sunlight exposure reduced the coloured DOM and carbon signals, which was followed by a production of inorganic nutrients. Bacterial carbon cycling was higher in the dark compared with the light treatment in seawater and river samples, while higher levels were found in the sunlight-exposed eelgrass experiment. Sunlight pre-exposure stimulated the bacterial growth efficiency in the seawater experiments, while no impact was found in the other experiments. We suggest that these responses are connected to differences in substrate composition and the production of free radicals. The bacterial community that developed in the dark and sunlight pre-treated samples differed in the seawater and river experiments. Our findings suggest that impact of sunlight exposure on the bacterial carbon transfer and diversity depends on the DOM source and on the sunlight-induced production of inorganic nutrients.

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Contamination of coastal environments is often due to a complex mixture of pollutants, sometimes in trace levels, that may have significant effects on diversity and function of organisms. The aim of this study was to evaluate the short-term dynamics of bacterioplankton exposed to natural and artificial mixtures of contaminants. Bacterial communities from a southwestern Mediterranean ecosystem, lagoon and the bay (offshore) of Bizerte were exposed to i) elutriate from resuspension of contaminated sediment, and ii) an artificial mixture of metals and herbicides mimicking the contamination observed during sediment resuspension. Elutriate incubation as well as artificial spiking induced strong enrichments in nutrients (up to 18 times), metals (up to six times) and herbicides (up to 20 times) relative to the in situ concentrations in the offshore station, whereas the increases in contaminants were less marked in the lagoon station. In the offshore waters, the artificial mixture of pollutants provoked a strong inhibition of bacterial abundance, production and respiration and significant modifications of the potential functional diversity of bacterioplankton with a strong decrease of the carbohydrate utilization. In contrast, incubation with elutriate resulted in a stimulation of bacterial activities and abundances, suggesting that the toxic effects of pollutants were modified by the increase in nutrient and DOM concentrations due to the sediment resuspension. The effects of elutriate and the artificial mixture of pollutants on bacterial dynamics and the functional diversity were less marked in the lagoon waters, than in offshore waters, suggesting a relative tolerance of lagoon bacteria against contaminants.

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We evaluated in situ rates of bacterial carbon processing in Amazonian floodplain lakes and mainstems, during both high water (HW) and low water (LW) phases (p < 0.05). Our results showed that bacterial production (BP) was lower and more variable than bacterial respiration, determined as total respiration. Bacterial carbon demand was mostly accounted by BR and presented the same pattern that BR in both water phases. Bacterial growth efficiency (BGE) showed a wide range (0.2-23%) and low mean value of 3 and 6%, (in HW and LW, respectively) suggesting that dissolved organic carbon was mostly allocated to catabolic metabolism. However, BGE was regulated by BP in LW phase. Consequently, changes in BGE showed the same pattern that BP. In addition, the hydrological pulse effects on mainstems and floodplains lakes connectivity were found for BP and BGE in LW. Multiple correlation analyses revealed that indexes of organic matter (OM) quality (chlorophyll-a, N stable isotopes and C/N ratios) were the strongest seasonal drivers of bacterial carbon metabolism. Our work indicated that: (i) the bacterial metabolism was mostly driven by respiration in Amazonian aquatic ecosystems resulting in low BGE in either high or LW phase; (ii) the hydrological pulse regulated the bacterial heterotrophic metabolism between Amazonian mainstems and floodplain lakes mostly driven by OM quality.

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Bacterial metabolism plays a dual role [bacterial production (BP) and bacterial respiration (BR)] in the aquatic ecosystem and potentially leads to hypoxia in the coastal eutrophic area. Bacterial growth efficiency (BGE) is an important index showing the contribution of bacterial metabolism to marine biological production and carbon budget in the pelagic ecosystem. In this study, the spatial and seasonal variety as well as diurnal variation dynamics of BGE and associated ecological characteristics were investigated in a partly eutrophicated subtropical bay (the Daya Bay) located in the northern South China Sea. Furthermore, the relationship between bacterial metabolism and potential hypoxia event was analyzed. The average BGE was 0.14 and 0.22 in summer and winter, respectively, which was lower than the mean value ever reported in other coastal and estuarine waters. The diurnal variations of BGE and BP were widely fluctuated in the Daya Bay, with approximately 3-8 fold variation of BP and 2-3 fold variation of BR in different seasons, suggesting the importance of short-term ecological dynamics on evaluating the long-term ecological processes in the coastal waters. BR was the predominant contributor to the bacterial carbon demand; however, the variation of BGE was controlled by BP in both seasons. BGE was always high in the near-shore waters with higher eutrophic level and more active BP and BR. The bacterial metabolism could deplete dissolved oxygen (DO) in the Daya bay within about 9 days when the water body was enclosed and photosynthesis was prohibited. Therefore, low DO concentration and potential hypoxia was more likely to be found in the near-shore waters of the Daya Bay in summer, since the water was stratified and enclosed with poor water exchange capacity in this area. While in winter, hypoxia seldom occurred due to vertical mixing throughout the water column. Further biological-physical coupling research is recommended to find out the detailed formation mechanism of hypoxia in the bay, and to predict the potential hypoxia events and their environmental impacts in the future.

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Temperature and nutrient concentrations regulate aquatic bacterial metabolism. However, few studies have focused on the effect of the interaction between these factors on bacterial processes, and none have been performed in tropical aquatic ecosystems. We analyzed the main and interactive effects of changes in water temperature and N and P concentrations on bacterioplankton production (BP), bacterioplankton respiration (BR) and bacterial growth efficiency (BGE) in tropical coastal lagoons. We used a factorial design with three levels of water temperature (25, 30, and 35°C) and four levels of N and/or P additions (Control, N, P, and NP additions) in five tropical humic lagoons. When data for all lagoons were pooled together, a weak interaction was observed between the increase in water temperature and the addition of nutrients. Water temperature alone had the greatest impact on bacterial metabolism by increasing BR, decreasing BP, and decreasing BGE. An increase of 1°C lead to an increase of ~4% in BR, a decrease of ~0.9% in BP, and a decrease of ~4% in BGE. When data were analyzed separately, lagoons responded differently to nutrient additions depending on Dissolved Organic Carbon (DOC) concentration. Lagoons with lowest DOC concentrations showed the strongest responses to nutrient additions: BP increased in response to N, P, and their interaction, BR increased in response to N and the interaction between N and P, and BGE was negatively affected, mainly by the interaction between N and P additions. Lagoons with the highest DOC concentrations showed almost no significant relationship with nutrient additions. Taken together, these results show that different environmental drivers impact bacterial processes at different scales. Changes of bacterial metabolism related to the increase of water temperature are consistent between lagoons, therefore their consequences can be predicted at a regional scale, while the effect of nutrient inputs is specific to different lagoons but seems to be related to the DOC concentration.