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Bacteria-organic matter coupling and its significance for oceanic carbon cycling
Abstract
This paper synthesizes current ideas on the role of the microbial loop in carbon fluxes in the ocean and proposes some directions for future research. Organic matter flux into bacteria is highly variable, which can significantly influence the pathways of carbon flow in the ocean. A goal for future research is to elucidate the mechanistic bases of bacteria-organic matter coupling. This research should take into consideration the micrometer-scale distribution of bacteria and the composition, structure, and dynamics of the organic matter field in the bacterium's microhabitat. The ideas on the interactions of bacteria with the particulate organic phase need to be revised in view of recent findings of highly abundant, previously unknown particles ranging in size from nanometers to hundreds of micrometers. The "hot-spots" in the distribution of organic matter and remineralized nutrients can influence the rates as well as the direction of biogeochemical fluxes. Slow-to-degrade dissolved organic matter (DOM) may be produced because of loose bacteria-organic matter coupling resulting in DOM storage. Its use at a later time and place has profound implications for carbon fluxes and food web dynamics. A fundamental research need for the future is to understand the ecological interactions among the members of the microbial loop in an appropriate microhabitat context. While this goal was previously intractable, new molecular and optical techniques should make it possible to understand the biogeochemical activities of the microbial loop in terms of the ecology and evolution of pelagic microbial communities.
... While the exchange of chemical currencies between phytoplankton and their phycosphere constituents has long been recognized as a key contributing factor to aquatic ecosystem dynamics (Azam et al, 1994;Paerl, 1975), the extent of their impact and potential role in the occurrence symptoms of dysbiosis, such as harmful algal blooms (HABs) has only recently been recognized Seymour et al, 2017). ...
... (including bacteria and archaea, hereinafter referred to as bacteria) have a paramount role in turning such cycles, by e.g., mediating the remineralization of massive amounts of dissolved organic carbon produced daily by primary producers (Boyd et al. 1999;Robinson and Williams n.d.) and controlling fluxes of energy in the ocean (Farooq Azam 1998;F. Azam et al. 1994;le B. Williams and J 1998). Thus, a key question is how temperature impacts fundamental aspects of bacterial metabolism in oceanic waters. The analysis of temperature effects on bulk bacterial metabolic rates, including biomass production, respiration, or enzymatic activity has been the focus of a number of studies (see for example White ...
Temperature stands as one of the key factors influencing the community structure and distribution of marine microorganisms. Yet, the physiological adaptations of marine bacteria to rising temperatures remain underexplored. This study examines the transcriptional response of Dokdonia sp. MED134, a proteorhodopsin-based phototrophic organism within the class Flavobacteriia, to a gradient of temperature acclimation conditions from 10 to 34C. Light availability during day/night cycles exerted minimal influence on the transcriptional patterns of this strain, with only a few genes mostly related to light sensing, light protecting mechanisms and phototrophy being upregulated during daytime. By contrast, temperature significantly impacted the expression of a large fraction of MED134 genes (>60%), including components of the stress response, cellular translation, DNA replication, and some metabolic pathways such as the anaplerotic carbon fixation and the glyoxylate shunt, suggesting intracellular carbon flow adjustments to temperature. Notably, the expression of some highly expressed TonB transporters, prominent in flavobacteria, was also temperature-sensitive. Our findings provide insights into the transcriptional adjustments of Dokdonia sp. MED134 in response to temperature variations, suggesting potential implications for carbon cycling and organic matter processing in marine environments.
... 47, 56-58 Primary production in aquatic systems also generates autochthonous particulate and dissolved OC, further complicating the cycling of organic carbon. 59,60 Evidence indicates that the stocks, fluxes, and functions of OC in aquatic systems are vulnerable to human activities and climate-driven perturbations. [61][62][63][64] Land-cover disturbance, warming and thawing of soils, changing hydrology, and degradation of wetlands are all environmental perturbations influencing the mobilization and processing of terrigenous OC waters and its influx to the coastal ocean. ...
... molecules, dominated by Rhodobacterales 9 . In both cases, the primary mechanisms for degradation and uptake involve extracellular enzymes and transporters 10 , and many resources now exist to identify genes involved in such processes, including polysaccharide 11 and protein 12 degradation. Compounds released by bacteria and known to be reincorporated by photoautotrophs for biomass include ammonium 5 , amino acids 13 , and carbon dioxide 14 . ...
Bacterial remineralization of algal organic matter fuels algal growth but is rarely quantified. Consequently, we cannot currently predict whether some bacterial taxa may provide more remineralized nutrients to algae than others. Here, we quantified bacterial incorporation of algal-derived complex dissolved organic carbon and nitrogen and algal incorporation of remineralized carbon and nitrogen in fifteen bacterial co-cultures growing with the diatom Phaeodactylum tricornutum at the single-cell level using isotope tracing and nanoSIMS. We found unexpected strain-to-strain and cell-to-cell variability in net carbon and nitrogen incorporation, including non-ubiquitous complex organic nitrogen utilization and remineralization. We used these data to identify three distinct functional guilds of metabolic interactions, which we termed macromolecule remineralizers, macromolecule users, and small-molecule users, the latter exhibiting efficient growth under low carbon availability. The functional guilds were not linked to phylogeny and could not be elucidated strictly from metabolic capacity as predicted by comparative genomics, highlighting the need for direct activity-based measurements in ecological studies of microbial metabolic interactions.
... However, oceanic trenches have been described as depocenters of OM (Danovaro et al., 2003) and hotspots for heterotrophic microbial activity (Glud et al., 2013;Liu et al., 2019;Luo et al., 2018;Wenzhöfer et al., 2016). The coupling between microbial activity and OM availability is important for nutrient remineralization, which can in turn influence the rates and directions of biogeochemical fluxes (Azam et al., 1994). Thus, elevated concentrations of OM in trench sediments could be explained by more diverse sources of energy feeding the hadal environment. ...
Oceanic trenches are an important sink for organic matter (OM). However, little is known about how much of the OM reaching the hadal region derives from the sunlit surface ocean and other sources. We provide new insight into the OM sources in the Atacama Trench by examining the elemental and stable isotope composition of carbon and nitrogen in bulk OM throughout the entire water column and down to bathyal and hadal sediments. Moreover, we estimated the particulate organic carbon (POC) concentration and downward carbon flux. Our results, based on two‐way variance analysis, showed statistical differences in δ¹⁵NPON between the epipelagic zone and the deep zones. However, no statistical differences in δ¹³CPOC and C:N ratio between hadalpelagic and shallower pelagic zones were found, except for δ¹³CPOC in the oxygen‐deficient zone. On the contrary, whereas the isotopic signatures of hadal sediments were distinct from those over the entire water column, they were similar to the values in bathyal sediments. Thus, our results suggest that bathyal sediments could contribute more OM to hadal sediments than the different zones of the water column. Indeed, whereas POC flux estimates derived from remote sensing data indicate that ∼16%–27% of POC could evade surface remineralization within the top 200 m and potentially be exported to depths beyond the mesopelagic region, model estimates suggest that ∼3.3% of it could reach hadal depths. Our results provide a quantitative baseline of pelagic‐benthic coupling which can aid in assessment of carbon cycling changes in future climate scenarios.
... Much of the efficient recycling of phytoplankton-derived organic matter in the ocean is due to heterotrophic microbial communities, which consume, transform, excrete, and respire an estimated half of autochthonously-produced organic matter (Azam et al., 1993;Azam and Malfatti, 2007). The depths and rates at which this organic matter is respired and transformed affects the major biogeochemical cycles of carbon and nutrients, which help determine the distribution of heterotrophic life in the ocean (Hutchins and Fu, 2017). ...
... Total organic carbon is comprised of a dissolved (DOC) and particulate (POC) phase and is often used as a proxy measurement for organic matter concentration in aquatic studies (as reviewed in [28]). Furthermore, the quality and quantity of TOC is known to influence the growth [29] and community composition [30,31] of aquatic bacteria. Measurements of precontact rainwater TOC (or DOC) are sparse, with reported values from ten studies ranging from 10.0 μM C-779.0 μM C (see S1 Table and Siudek at al. 2015 [32]). ...
Rain contains encapsulated bacteria that can be transported over vast distances during relatively short periods of time. However, the ecological significance of bacteria in "precontact" rainwater-rainwater prior to contact with non-atmospheric surfaces-remains relatively undefined given the methodological challenges of studying low-abundance microbes in a natural assemblage. Here, we implement single-cell "click" chemistry in a novel application to detect the protein synthesis of bacteria in precontact rainwater samples as a measure of metabolic activity. Using epifluorescence microscopy, we find approximately 103-104 bacteria cells mL-1 with up to 7.2% of the observed cells actively synthesizing protein. Additionally, our measurement of less than 30 μM total organic carbon in the samples show that some rainwater bacteria can metabolize substrates in very low organic matter conditions, comparable to extremophiles in the deep ocean. Overall, our results raise new questions for the field of rainwater microbiology and may help inform efforts to develop quantitative microbial risk assessments for the appropriate use of harvested rainwater.
... 2007). Coastal systems are productive regions and therefore also generate autochthonous DOC indirectly from primary production through the microbial loop (Anderson and Ducklow, 2001;Azam et al., 1994). Overall, 0.15-0.35 ...
... Alphaproteobacteria and Gammaproteobacteria showed the same trend, decreasing from spring to the summer and then increasing in the winter. Proteobacteria (Alpha, Gamma, and Delta) have diverse metabolic pathways that are critical for nutrient cycling, conversion, and the remineralization of substances such as organic carbon and nitrogen [26][27][28]. Alphaproteobacteria is generally abundant in marine waters [29,30]. Figure 4b shows relatively small differences in the abundance of Alphaproteobacteria across the seasons. ...
Planktonic cells are a vital part of biogeochemical nutrient cycling and play an extremely important role in maintaining the balance of water ecosystems. In this study, surface water samples were collected in three seasons (spring, summer, and winter) 10 km along the estuary of the Bailang River to assess the relationship between environmental factors and the bacterial community structure, which was determined by high-throughput sequencing. The physicochemical properties of the samples, including the pH, salinity, and inorganic nitrogen (NH4+, NO3−, and NO2−), exhibited significant seasonal variations, and the diversity and structure of the bacterial community also varied seasonally. A redundancy analysis showed that the inorganic nitrogen (NH4+, NO3−, NO2−), pH, and salinity are key factors in shaping the bacterial community composition. Among the different seasons, the core taxa of bacterial communities were the same, and Actinobacteria, Cyanobacteria, and Proteobacteria were the key components during the three seasons. The bacterial diversity and structure also varied seasonally, but there were no significant differences in spatial composition. Based on a phylogenetic investigation of communities by reconstruction of unobserved states analysis, nitrogen-cycle-related processes include four dominant processes: nitrogen mineralization, nitrogen fixation, dissimilatory nitrate reduction, and denitrification. These results suggest that the bacterial community structure in the waters of the Bailang River estuary is subject to seasonal rather than spatial variation. These findings provide new evidence for studies of the seasonal variation of bacterial communities in estuaries.
Rubber plantations are an important component of tropical forest ecosystems and are emerging as crucial contributors to carbon sequestration in the tropics. However, ecosystem respiration (RECO), which constitutes an essential constraint on the carbon fixation capacity of rubber plantations, and its driving mechanisms remains unclear. Therefore, this study developed a data-driven semi-empirical model to simulate rubber plantations RECO utilising eddy covariance flux measurements and was upscaled to Hainan Island using remote sensing images and climatic data. Numerical simulations experiments analysed direct and indirect of climatic factors impacts on rubber plantations RECO. The results showed that the model accurately captured RECO trends and seasonality (R2 = 0.87, RMSE = 1.27 g C m−2 d−1); in the past 19 years, RECO showed a noticeable increase, particularly in the late rainy season and the seasonality of RECO has shown a delayed pattern. The RECO in the central region (52% area) exhibited multimodal enhancement while northern and southern regions (37% area) showed oscillations or decreases. Temporally, RECO is higher in the rainy season compared to the dry season, and spatially, RECO is higher in the southern region than in the northern region. Among the climatic factors, water conditions (rainfall and air humidity) have been emerged as dominant factors (5.38%) influencing RECO, surpassing temperature (3.96%) and radiation (3.81%). In addition, climatic factors make a positive overall contribution during the dry season but perform oppositely in the rainy season. This study offers theoretical and technical insights into high carbon sink management in rubber plantations and carbon sequestration in tropical forests ecosystems.
Differential filtration and multiple isotopic labeling were combined to study the uptake of [14C]bicarbonate, [14C]glucose, and [32P]orthophosphate by microplakton in Lake Kinneret, Israel. Short-term (4 hr) uptake experiments showed seasonal changes in the size distributions of organisms taking up inorganic carbon, glucose carbon, and orthophosphate in the lake water. In a time-course experiment of 48 hr (Jan 1976) most, but not all, of the photosynthetic activity (average 72%) and a similar fraction of chlorophyll (72%) were associated with organisms retained on 3-m Nuclepore filters (retention on 0.4-m filters was 100%). About 90% of the organisms that assimilated glucose passed through 3-m filters. Photosynthetic carbon fixation, dark carbon uptake, and heterotrophic uptake of glucose carbon accounted for 99%, 1%, and 1%, respectively, of the total net carbon assimilated during the first 6 hours. Radioactive phosphorus showed an initial rapid uptake into particles, which was not affected by light or dark. We suggest that this methodology has a wide potential for elucidating the flux of nutrients into various components of the microplankton and in characterizing different aquatic environments.
Recently developed methods for measuring production rates of heterotrophic bacteria have shown that the bacterioplankton is a major route for the flux of material and energy in marine ecosystems (Hagström et al., 1979; Fuhrman and Azam, 1980, 1982; Williams, 1981). Even conservative estimates (Fuhrman and Azam, 1980, 1982) show that the measured bacterial productivity corresponds to 10–50% of the primary productivity.
Traditionally, the only component of the microbial communities studied seriously by biological oceanographers was phytoplankton. Bacteria, protozoa, viruses and fungi were relegated to “specialists” and it was implicitly assumed that, by and large, the ocean’s productivity mechanisms and biogeochemical dynamics could be understood and modelled without taking into account the activities of these other components of the pelagic microbiota. This view was challenged by the seminal paper of Pomeroy (1974) and by quantitative studies inspired by it, leading up to the discovery that the pathway DOM -- > bacteria -- > protozoa -- > metazoa (microbial loop; Azam et al., 1983) is a major route for the flows of material and energy in pelagic marine ecosystems. Further, very recently it has been suggested that viruses may also play important ecological roles (Bergh et al., 1989; Proctor and Fuhrman, 1990; Suttle et al., 1990), including a role in the mortality of bacteria and phytoplankton.