Paul A. del Giorgio

Respiration in the open ocean

A key question when trying to understand the global carbon cycle is whether the oceans are net sources or sinks of carbon. This will depend on the production of organic matter relative to the decomposition due to biological respiration. Estimates of respiration are available for the top layers, the mesopelagic layer, and the abyssal waters and sediments of various ocean regions. Although the total open ocean respiration is uncertain, it is probably substantially greater than most current estimates of particulate organic matter production. Nevertheless, whether the biota act as a net source or sink of carbon remains an open question.

Methane fluxes show consistent temperature dependence across microbial to ecosystem scales

Methane (CH4) is an important greenhouse gas because it has 25 times the global warming potential of carbon dioxide (CO2) by mass over a century. Recent calculations suggest that atmospheric CH4 emissions have been responsible for approximately 20% of Earth’s warming since pre-industrial times. Understanding how CH4 emissions from ecosystems will respond to expected increases in global temperature is therefore fundamental to predicting whether the carbon cycle will mitigate or accelerate climate change. Methanogenesis is the terminal step in the remineralization of organic matter and is carried out by strictly anaerobic Archaea. Like most other forms of metabolism, methanogenesis is temperature-dependent. However, it is not yet known how this physiological response combines with other biotic processes (for example, methanotrophy, substrate supply, microbial community composition) and abiotic processes (for example, water-table depth) to determine the temperature dependence of ecosystem-level CH4 emissions. It is also not known whether CH4 emissions at the ecosystem level have a fundamentally different temperature dependence than other key fluxes in the carbon cycle, such as photosynthesis and respiration. Here we use meta-analyses to show that seasonal variations in CH4 emissions from a wide range of ecosystems exhibit an average temperature dependence similar to that of CH4 production derived from pure cultures of methanogens and anaerobic microbial communities. This average temperature dependence (0.96 electron volts (eV)), which corresponds to a 57-fold increase between 0 and 30°C, is considerably higher than previously observed for respiration (approximately 0.65 eV) and photosynthesis (approximately 0.3 eV). As a result, we show that both the emission of CH4 and the ratio of CH4 to CO2 emissions increase markedly with seasonal increases in temperature. Our findings suggest that global warming may have a large impact on the relative contributions of CO2 and CH4 to total greenhouse gas emissions from aquatic ecosystems, terrestrial wetlands and rice paddies.

LINKING PLANKTONIC BIOMASS AND METABOLISM TO NET GAS FLUXES IN NORTHERN TEMPERATE LAKES

Plankton communities in oligotrophic waters are characteristically dominated by the biomass of heterotrophs, including bacteria, micro-, and macrozooplankton. It has been generally assumed that these inverted biomass pyramids are the direct result of high specific production rates of phytoplankton and a tight coupling between producers and consumers. There are, however, at least two alternative hypotheses: (1) heterotrophic biomass turnover is much slower in oligotrophic than eutrophic systems; and (2) oligotrophic planktonic communities are significantly subsidized by allochthonous organic matter. In this study we assessed these hypotheses by establishing the relationship between plankton biomass structure (partition between auto- and heterotrophs), plankton function (plankton primary production and respiration) and whole-lake gas (O2 and CO2) fluxes in 20 temperate lakes that span a large range in primary production. We show that the balance of phytoplankton production and community respiration (P/R rat...

Reconciling the temperature dependence of respiration across timescales and ecosystem types

Ecosystem respiration is the biotic conversion of organic carbon to carbon dioxide by all of the organisms in an ecosystem, including both consumers and primary producers. Respiration exhibits an exponential temperature dependence at the subcellular and individual levels, but at the ecosystem level respiration can be modified by many variables including community abundance and biomass, which vary substantially among ecosystems. Despite its importance for predicting the responses of the biosphere to climate change, it is as yet unknown whether the temperature dependence of ecosystem respiration varies systematically between aquatic and terrestrial environments. Here we use the largest database of respiratory measurements yet compiled to show that the sensitivity of ecosystem respiration to seasonal changes in temperature is remarkably similar for diverse environments encompassing lakes, rivers, estuaries, the open ocean and forested and non-forested terrestrial ecosystems, with an average activation energy similar to that of the respiratory complex (approximately 0.65 electronvolts (eV)). By contrast, annual ecosystem respiration shows a substantially greater temperature dependence across aquatic (approximately 0.65 eV) versus terrestrial ecosystems (approximately 0.32 eV) that span broad geographic gradients in temperature. Using a model derived from metabolic theory, these findings can be reconciled by similarities in the biochemical kinetics of metabolism at the subcellular level, and fundamental differences in the importance of other variables besides temperature—such as primary productivity and allochthonous carbon inputs—on the structure of aquatic and terrestrial biota at the community level.

Factors influencing the detection of bacterial cells using fluorescence in situ hybridization (FISH): A quantitative review of published reports.

Abstract Fluorescence in situ hybridization (FISH) is widely used to describe bacterial community composition and, to a lesser extent, to describe the physiological state of cells. One of the limitations of the technique is that the effectiveness of the detection of target cells appears to vary widely. Here, we present a quantitative review of published reports on the percentage of cells detected using the common EUB338 probe (%Eub) in aquatic ecosystems. The %Eub varies from 1 to 100% in the different published reports, with an average of 56%. There is a methodological component in this variation, with a significant effect of the fluorochrome type and the stringency conditions of the reaction. But there is also a strong environmental component, and the type of ecosystem and dominant phylogenetic group significantly influence %Eub. We argue that the optimization of the FISH protocol to describe the phylogenetic composition of bacterial assemblages will probably lead to techniques that are not effective to describe the physiological state of cells.

What’s in an EEM? Molecular Signatures Associated with Dissolved Organic Fluorescence in Boreal Canada

Dissolved organic matter (DOM) is a master variable in aquatic systems. Modern fluorescence techniques couple measurements of excitation emission matrix (EEM) spectra and parallel factor analysis (PARAFAC) to determine fluorescent DOM (FDOM) components and DOM quality. However, the molecular signatures associated with PARAFAC components are poorly defined. In the current study we characterized river water samples from boreal Québec, Canada, using EEM/PARAFAC analysis and ultrahigh resolution mass spectrometry (FTICR-MS). Spearmans correlation of FTICR-MS peak and PARAFAC component relative intensities determined the molecular families associated with 6 PARAFAC components. Molecular families associated with PARAFAC components numbered from 39 to 572 FTICR-MS derived elemental formulas. Detailed molecular properties for each of the classical humic- and protein-like FDOM components are presented. FTICR-MS formulas assigned to PARAFAC components represented 39% of the total number of formulas identified and 59% of total FTICR-MS peak intensities, and included significant numbers compounds that are highly unlikely to fluoresce. Thus, fluorescence measurements offer insight into the biogeochemical cycling of a large proportion of the DOM pool, including a broad suite of unseen molecules that apparently follow the same gradients as FDOM in the environment.

Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems.

Jellyfish blooms occur in many estuarine and coastal regions and may be increasing in their magnitude and extent worldwide. Voracious jellyfish predation impacts food webs by converting large quantities of carbon (C), fixed by primary producers and consumed by secondary producers, into gelatinous biomass, which restricts C transfer to higher trophic levels because jellyfish are not readily consumed by other predators. In addition, jellyfish release colloidal and dissolved organic matter (jelly-DOM), and could further influence the functioning of coastal systems by altering microbial nutrient and DOM pathways, yet the links between jellyfish and bacterioplankton metabolism and community structure are unknown. Here we report that jellyfish released substantial quantities of extremely labile C-rich DOM, relative to nitrogen (25.6 ± 31.6 C:1N), which was quickly metabolized by bacterioplankton at uptake rates two to six times that of bulk DOM pools. When jelly-DOM was consumed it was shunted toward bacterial respiration rather than production, significantly reducing bacterial growth efficiencies by 10% to 15%. Jelly-DOM also favored the rapid growth and dominance of specific bacterial phylogenetic groups (primarily γ-proteobacteria) that were rare in ambient waters, implying that jelly-DOM was channeled through a small component of the in situ microbial assemblage and thus induced large changes in community composition. Our findings suggest major shifts in microbial structure and function associated with jellyfish blooms, and a large detour of C toward bacterial CO2 production and away from higher trophic levels. These results further suggest fundamental transformations in the biogeochemical functioning and biological structure of food webs associated with jellyfish blooms.

Increases in terrestrially derived carbon stimulate organic carbon processing and CO2 emissions in boreal aquatic ecosystems

The concentrations of terrestrially derived dissolved organic carbon have been increasing throughout northern aquatic ecosystems in recent decades, but whether these shifts have an impact on aquatic carbon emissions at the continental scale depends on the potential for this terrestrial carbon to be converted into carbon dioxide. Here, via the analysis of hundreds of boreal lakes, rivers and wetlands in Canada, we show that, contrary to conventional assumptions, the proportion of biologically degradable dissolved organic carbon remains constant and the photochemical degradability increases with terrestrial influence. Thus, degradation potential increases with increasing amounts of terrestrial carbon. Our results provide empirical evidence of a strong causal link between dissolved organic carbon concentrations and aquatic fluxes of carbon dioxide, mediated by the degradation of land-derived organic carbon in aquatic ecosystems. Future shifts in the patterns of terrestrial dissolved organic carbon in inland waters thus have the potential to significantly increase aquatic carbon emissions across northern landscapes.

Biomass Distribution in Freshwater Plankton Communities

Both resource control of heterotrophic biomass and heterotrophic regulation of plant populations imply that heterotrophic biomass should constitute an increasingly smaller proportion of total system biomass as the turnover time of autotrophs increases. Although this trend is widely accepted, it has seldom been tested, perhaps because comparable data for many ecosystems are hard to collect. The plankton are an exception to this difficulty. Because the biomasses of both autotrophs and heterotrophs can be estimated with relative ease and because workers use similar techniques, data are available from a wide range of lakes. Both literature data, representing a wide geographical range, and data from a localized set of lakes show that the ratio of heterotrophic to autotrophic biomass (H/A ratio) is well above unity where autotrophic biomass is low and declines where autotrophic biomass is high. A similar pattern is found in marine and terrestrial systems In terrestrial systems, this pattern has been explained by changes in the turnover time of the autotrophic biomass, but in lakes energetic subsidies from the littoral and the watershed are likely needed to support the relatively high heterotrophic biomass of many oligotrophic systems.

Magnitude and regulation of bacterioplankton respiratory quotient across freshwater environmental gradients

Bacterioplankton respiration (BR) may represent the largest single sink of organic carbon in the biosphere and constitutes an important driver of atmospheric carbon dioxide (CO2) emissions from freshwaters. Complete understanding of BR is precluded by the fact that most studies need to assume a respiratory quotient (RQ; mole of CO2 produced per mole of O2 consumed) to calculate rates of BR. Many studies have, without clear support, assumed a fixed RQ around 1. Here we present 72 direct measurements of bacterioplankton RQ that we carried out in epilimnetic samples of 52 freshwater sites in Québec (Canada), using O2 and CO2 optic sensors. The RQs tended to converge around 1.2, but showed large variability (s.d.=0.45) and significant correlations with major gradients of ecosystem-level, substrate-level and bacterial community-level characteristics. Experiments with natural bacterioplankton using different single substrates suggested that RQ is intimately linked to the elemental composition of the respired compounds. RQs were on average low in net autotrophic systems, where bacteria likely were utilizing mainly reduced substrates, whereas we found evidence that the dominance of highly oxidized substrates, for example, organic acids formed by photo-chemical processes, led to high RQ in the more heterotrophic systems. Further, we suggest that BR contributes to a substantially larger share of freshwater CO2 emissions than presently believed based on the assumption that RQ is ∼1. Our study demonstrates that bacterioplankton RQ is not only a practical aspect of BR determination, but also a major ecosystem state variable that provides unique information about aquatic ecosystem functioning.