Integrating terrestrial and aquatic ecosystems to constrain estimates of land-atmosphere carbon exchange.

In this Perspective, we put forward an integrative framework to improve estimates of land-atmosphere carbon exchange based on the accumulation of carbon in the landscape as constrained by its lateral export through rivers. The framework uses the watershed as the fundamental spatial unit and integrates all terrestrial and aquatic ecosystems as well as their hydrologic carbon exchanges. Application of the framework should help bridge the existing gap between land and atmosphere-based approaches and offers a platform to increase communication and synergy among the terrestrial, aquatic, and atmospheric research communities that is paramount to advance landscape carbon budget assessments.

Catchment-scale carbon fluxes and processes in major rivers of northern Québec, Canada.

Boreal rivers transport and process large amounts of organic and inorganic materials derived from their catchments, yet quantitative estimates and patterns of carbon (C) transport and emissions in these large rivers are scarce relative to those of high-latitude lakes and headwater streams. Here, we present the results of a large-scale survey of 23 major rivers in northern Québec sampled during the summer period of 2010, which aimed to determine the magnitude and spatial variability of different C species (carbon dioxide - CO2, methane - CH4, total carbon - TC, dissolved organic carbon - DOC and inorganic carbon - DIC), as well as to identify their main drivers. In addition, we constructed a first order mass balance of total riverine C emissions to the atmosphere (outgassing from the main river channel) and export to the ocean over summer. All rivers were supersaturated in pCO2 and pCH4 (partial pressure of CO2 and CH4), and the resulting fluxes varied widely among rivers, especially the CH4. There was a positive relationship between DOC and gas concentrations, suggesting a common watershed source of these C species. DOC concentrations declined as a function of % land surface covered by water (lentic + lotic systems) in the watershed, suggesting that lentic systems may act as a net sink of organic matter in the landscape. The C balance suggests that the export component is higher than atmospheric C emissions in the river channel. However, for heavily dammed rivers, C emissions to the atmosphere approaches the C export component. Such studies are highly important for the overall efforts to effectively quantify and incorporate major boreal rivers into whole-landscape C budgets, to determine the net role of these ecosystems as C sinks or sources, and to predict how these might shift under anthropogenic pressures and dynamic climate conditions.

Terrestrial connectivity, upstream aquatic history and seasonality shape bacterial community assembly within a large boreal aquatic network.

During transit from soils to the ocean, microbial communities are modified and re-assembled, generating complex patterns of ecological succession. The potential effect of upstream assembly on downstream microbial community composition is seldom considered within aquatic networks. Here, we reconstructed the microbial succession along a land-freshwater-estuary continuum within La Romaine river watershed in Northeastern Canada. We captured hydrological seasonality and differentiated the total and reactive community by sequencing both 16 S rRNA genes and transcripts. By examining how DNA- and RNA-based assemblages diverge and converge along the continuum, we inferred temporal shifts in the relative importance of assembly processes, with mass effects dominant in spring, and species selection becoming stronger in summer. The location of strongest selection within the network differed between seasons, suggesting that selection hotspots shift depending on hydrological conditions. The unreactive fraction (no/minor RNA contribution) was composed of taxa with diverse potential origins along the whole aquatic network, while the majority of the reactive pool (major RNA contribution) could be traced to soil/soilwater-derived taxa, which were distributed along the entire rank-abundance curve. Overall, our findings highlight the importance of considering upstream history, hydrological seasonality and the reactive microbial fraction to fully understand microbial community assembly on a network scale.

Tracking the upstream history of aquatic microbes in a boreal lake yields new insights on microbial community assembly.

Bacterial community structure can change rapidly across short spatial and temporal scales as environmental conditions vary, but the mechanisms underlying those changes are still poorly understood. Here, we assessed how a lake microbial community assembles by following its reorganization from the main tributary, which, when flowing into the lake, first traverses an extensive macrophyte-dominated vegetated habitat, before reaching the open water. Environmental conditions in the vegetated habitat changed drastically compared to both river and lake waters and represented a strong environmental gradient for the incoming bacteria. We used amplicon sequencing of the 16S rRNA gene and transcript to reconstruct the shifts in relative abundance of individual taxa and link this to their pattern in activity (here assessed with RNA:DNA ratios). Our results indicate that major shifts in relative abundance were restricted mostly to rare taxa (<0.1% of relative abundance), which seemed more responsive to environmental changes. Dominant taxa (>1% of relative abundance), on the other hand, traversed the gradient mostly unchanged with relatively low and stable RNA:DNA ratios. We also identified a high level of local recruitment and a seedbank of taxa capable of activating/inactivating, but these were almost exclusively associated with the rare biosphere. Our results suggest a scenario where the lake community results from a reshuffling of the rank abundance structure within the incoming rare biosphere, driven by selection and growth, and that numerical dominance is not a synonym of activity, growth rate, or environmental selection, but rather reflect mass effects structuring these freshwater bacterial communities.

Freshwater zooplankton metapopulations and metacommunities respond differently to environmental and spatial variation.

Theory predicts that population genetic structure and metacommunity structure are linked by the common processes of drift and migration, but how population genetic structure and metacommunity structure are related in nature is still unknown. Deeper understanding of the processes influencing both genetic and community diversity is vital for better predicting how environmental change will impact biodiversity patterns. We examined how crustacean zooplankton and rotifer species' metapopulation genetic structure and metacommunities respond to environmental and spatial variation both within and across four regions of boreal Canada. Metapopulation and metacommunity variation partitioning results were compared within and across the four regions. Metapopulations and metacommunities responded differently to environmental variation and spatial structure both within and across regions, as metapopulations were influenced by different environmental variables compared to metacommunities. At larger spatial scales both metapopulations and metacommunities exhibited greater spatial and environmental structuring, again responding to a different subset of environmental variables. Our findings suggest that even though both genetic and species diversity are linked by the same processes, regional variation in environmental characteristics and spatial structure influence resulting biodiversity patterns differently. To date, no other empirical research has explored relationships between entire metapopulation and metacommunity assemblages at large regional spatial scales.

Comment on "On the calculation of lake metabolic rates: Diel O2 and 18/16O technique" by Peeters et al. [Water Res. 165 2019, 114990].

Quantifying metabolic rates in lakes and other aquatic ecosystems is a complex task, as methods are continually evolving and are not currently standardized. Recently, Peeters et al. presented a valuable simulated dataset that advances the field by comparing the strengths and limitations of individual and combined metabolic techniques. The authors conclude that calculating metabolic rates from point sampling and mass balancing of surface water oxygen concentration and isotope composition is flawed, because the technique does not capture sub-daily patterns of metabolic variability, which they argue invalidates past applications and interpretations. These conclusions are inconsistent with how the method has been used, and are based on a biased construction of scenarios and interpretation of model results, especially because their parameterization of the stable isotopic model employs input values that appear unrepresentative of most lake conditions. Here, we establish that 1) empirical evidence supports the isotopic approach's suitability to approximate daily or longer metabolic patterns in most lakes. 2) The authors' own simulations show agreement between metabolic estimates from point isotopic measurements and average metabolic rates under most scenarios. 3) The authors' invalidation of isotopic measurements are based on the most extreme model deviations observed in simulated hypereutrophic environments. While we welcome a critical evaluation of the isotopic approach, we argue that isotopic model uncertainty needs to be placed within an appropriate context. We emphasize that isotopic sampling and steady state metabolic modelling has a key role to play in constraining metabolic patterns in the global lake landscape, but that the research questions addressed with the method need to be commensurate with the limitations and uncertainties of the approach.

Taxonomic differences shape the responses of freshwater aerobic anoxygenic phototrophic bacterial communities to light and predation.

Aerobic anoxygenic phototrophic (AAP) bacteria are a phylogenetically diverse and ubiquitous group of prokaryotes that use organic matter but can harvest light using bacteriochlorophyll a. Although the factors regulating AAP ecology have long been investigated through field surveys, the few available experimental studies have considered AAPs as a group, thus disregarding the potential differential responses between taxonomically distinct AAP assemblages. Here, we used sequencing of the pufM gene to describe the diversity of AAPs in 10 environmentally distinct temperate lakes, and to investigate the taxonomic responses of AAP communities in these lakes when subjected to similar experimental manipulations of light and predator removal. The studied communities were clearly dominated by Limnohabitans AAP but presented a clear taxonomic segregation between lakes presumably driven by local conditions, which was maintained after experimental manipulations. Predation reduction (but not light exposure) caused significant compositional shifts across most assemblages, but the magnitude of these changes could not be clearly related to changes in bulk AAP abundances or taxonomic richness of AAP assemblages during experiments. Only a few operational taxonomic units, which differed taxonomically between lakes, were found to respond positively during experimental treatments. Our results highlight that different freshwater AAP communities respond differently to similar control mechanisms, highlighting that in-depth knowledge on AAP diversity is essential to understand the ecology and potential role of these photoheterotrophs.

Efficiency of crustacean zooplankton in transferring allochthonous carbon in a boreal lake.

Increased incorporation of terrestrial organic matter (t-OM) into consumer biomass (allochthony) is believed to reduce growth capacity. In this study, we examined the relationship between crustacean zooplankton allochthony and production in a boreal lake that displays strong seasonal variability in t-OM inputs. Contrary to our hypotheses, we found no effect of allochthony on production at the community and the species levels. The high-frequency seasonal sampling (time-for-space) allowed for estimating the efficiency of zooplankton in converting this external carbon source to growth. From the daily t-OM inputs in the lake (57-3,027 kg C/d), the zooplankton community transferred 0.2% into biomass (0.01-2.36 kg C/d); this level was of the same magnitude as the carbon transfer efficiency for algal-derived carbon (0.4%). In the context of the boundless carbon cycle, which integrates inland waters as a biologically active component of the terrestrial landscape, the use of the time-for-space approach for the quantifying of t-OM trophic transfer efficiency by zooplankton is a critical step toward a better understanding of the effects of increasing external carbon fluxes on pelagic food webs.

Magnitude and drivers of integrated fluvial network greenhouse gas emissions across the boreal landscape in Québec.

Streams and rivers are now recognized to be sites of intense carbon (C) emissions, yet the lack of C emission estimates that integrate beyond individual river systems has slowed their inclusion in landscape C budgets. Here we apply empirical models of CO2 and CH4 concentrations and gas exchange continuously along entire fluvial networks to derive the total fluvial CO2 and CH4 emissions in large (3000 to 30,000 km2) watersheds located across the boreal biome of Québec (Canada). We assess how total fluvial network C emissions vary with landscape and climate properties, and compare their magnitude to other components of the landscape C budget. The total fluvial network emissions expressed as per unit watershed area ranged from 0.7 to 29.2 g C m-2 yr-1 for CO2, and 4-1780 mg C m-2 yr-1 for CH4, and neither was related to watershed area or drainage density. Rather, watershed slope and terrestrial net productivity were major drivers of the integrated network fluvial emissions. We also show that steeper watersheds had a greater proportion of emissions relative to downstream export of C from the watershed. Integrated fluvial emissions are of the same magnitude as the terrestrial C sink, yet these two fundamental components of the boreal landscape C budget are not tightly coupled.

Large-scale biogeography and environmental regulation of methanotrophic bacteria across boreal inland waters.

Aerobic methanotrophic bacteria (methanotrophs) use methane as a source of carbon and energy, thereby mitigating net methane emissions from natural sources. Methanotrophs represent a widespread and phylogenetically complex guild, yet the biogeography of this functional group and the factors that explain the taxonomic structure of the methanotrophic assemblage are still poorly understood. Here, we used high-throughput sequencing of the 16S rRNA gene of the bacterial community to study the methanotrophic community composition and the environmental factors that influence their distribution and relative abundance in a wide range of freshwater habitats, including lakes, streams and rivers across the boreal landscape. Within one region, soil and soil water samples were additionally taken from the surrounding watersheds in order to cover the full terrestrial-aquatic continuum. The composition of methanotrophic communities across the boreal landscape showed only a modest degree of regional differentiation but a strong structuring along the hydrologic continuum from soil to lake communities, regardless of regions. This pattern along the hydrologic continuum was mostly explained by a clear niche differentiation between type I and type II methanotrophs along environmental gradients in pH, and methane concentrations. Our results suggest very different roles of type I and type II methanotrophs within inland waters, the latter likely having a terrestrial source and reflecting passive transport and dilution along the aquatic networks, but this is an unresolved issue that requires further investigation.

The NSERC Canadian Lake Pulse Network: A national assessment of lake health providing science for water management in a changing climate.

The distribution and quality of water resources vary dramatically across Canada, and human impacts such as land-use and climate changes are exacerbating uncertainties in water supply and security. At the national level, Canada has no enforceable standards for safe drinking water and no comprehensive water-monitoring program to provide detailed, timely reporting on the state of water resources. To provide Canada's first national assessment of lake health, the NSERC Canadian Lake Pulse Network was launched in 2016 as an academic-government research partnership. LakePulse uses traditional approaches for limnological monitoring as well as state-of-the-art methods in the fields of genomics, emerging contaminants, greenhouse gases, invasive pathogens, paleolimnology, spatial modelling, statistical analysis, and remote sensing. A coordinated sampling program of about 680 lakes together with historical archives and a geomatics analysis of over 80,000 lake watersheds are used to examine the extent to which lakes are being altered now and in the future, and how this impacts aquatic ecosystem services of societal importance. Herein we review the network context, objectives and methods.

Understanding how microbiomes influence the systems they inhabit.

Translating the ever-increasing wealth of information on microbiomes (environment, host or built environment) to advance our understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes that they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here, we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system-level processes that they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted using constituent taxa (community-aggregated traits) from those properties that cannot currently be predicted using constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these three categories of microbial characteristics and connect them with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.

Soils associated to different tree communities do not elicit predictable responses in lake bacterial community structure and function.

Freshwater bacterioplankton communities are influenced by the inputs of material and bacteria from the surrounding landscape, yet few studies have investigated how different terrestrial inputs affect bacterioplankton. We examined whether the addition of soils collected under various tree species combinations differentially influences lake bacterial communities. Lake water was incubated for 6 days following addition of five different soils. We assessed the taxonomic composition (16S rRNA gene sequencing) and metabolic activity (Biolog Ecoplates) of lake bacteria with and without soil addition, and compared these to initial soil communities. Soil bacterial assemblages showed a strong influence of tree composition, but such community differences were not reflected in the structure of lake communities that developed during the experiment. Bacterial taxa showing the largest abundance increases during incubation were initially present in both lake water and across most soils, and were related to Cytophagales, Burkholderiales and Rhizobiales. No clear metabolic profiles based on inoculum source were found, yet soil-amended communities used 60% more substrate than non-inoculated communities. Overall, we show that terrestrial inputs influence aquatic communities by stimulating the growth and activity of certain ubiquitous taxa distributed across the terrestrial-aquatic continuum, yet different forest soils did not cause predictable changes in lake bacterioplankton assemblages.

Effects of experimental nitrogen fertilization on planktonic metabolism and CO2 flux in a hypereutrophic hardwater lake.

Hardwater lakes are common in human-dominated regions of the world and often experience pollution due to agricultural and urban effluent inputs of inorganic and organic nitrogen (N). Although these lakes are landscape hotspots for CO2 exchange and food web carbon (C) cycling, the effect of N enrichment on hardwater lake food web functioning and C cycling patterns remains unclear. Specifically, it is unknown if different eutrophication scenarios (e.g., modest non point vs. extreme point sources) yield consistent effects on auto- and heterotrophic C cycling, or how biotic responses interact with the inorganic C system to shape responses of air-water CO2 exchange. To address this uncertainty, we induced large metabolic gradients in the plankton community of a hypereutrophic hardwater Canadian prairie lake by adding N as urea (the most widely applied agricultural fertilizer) at loading rates of 0, 1, 3, 8 or 18 mg N L-1 week-1 to 3240-L, in-situ mesocosms. Over three separate 21-day experiments, all treatments of N dramatically increased phytoplankton biomass and gross primary production (GPP) two- to six-fold, but the effects of N on autotrophs plateaued at ~3 mg N L-1. Conversely, heterotrophic metabolism increased linearly with N fertilization over the full treatment range. In nearly all cases, N enhanced net planktonic uptake of dissolved inorganic carbon (DIC), and increased the rate of CO2 influx, while planktonic heterotrophy and CO2 production only occurred in the highest N treatments late in each experiment, and even in these cases, enclosures continued to in-gas CO2. Chemical effects on CO2 through calcite precipitation were also observed, but similarly did not change the direction of net CO2 flux. Taken together, these results demonstrate that atmospheric exchange of CO2 in eutrophic hardwater lakes remains sensitive to increasing N loading and eutrophication, and that even modest levels of N pollution are capable of enhancing autotrophy and CO2 in-gassing in P-rich lake ecosystems.

Surface water CO2 concentration influences phytoplankton production but not community composition across boreal lakes.

Recent experimental evidence suggests that changes in the partial pressure of CO2 (pCO2 ), in concert with nutrient fertilisation, may result in increased primary production and shifted phytoplankton community composition that favours species lacking adaptations to low CO2 environments. It is not clear whether these results apply in ambient freshwaters, which are already often supersaturated in CO2 , and where phytoplankton structure and activity are under complex control of diverse local and regional factors. Here, we use a large-scale comparative study of 69 boreal lakes to explore the influence of existing CO2 gradients (c. 50-2300 µatm) on phytoplankton community composition and biomass production. While community composition did not respond to pCO2 gradients, gross primary production was enhanced, but only in lakes already supersaturated in CO2 , demonstrating that environmental context is key in determining pCO2 -phytoplankton interactions. We further argue that increased atmospheric CO2 is unlikely to influence phytoplanktonic composition and production in northern lakes.

Identifying the core seed bank of a complex boreal bacterial metacommunity.

Seed banks are believed to contribute to compositional changes within and across microbial assemblages, but the application of this concept to natural communities remains challenging. Here we describe the core seed bank of a bacterial metacommunity from a boreal watershed, using the spatial distribution of bacterial operational taxonomic units (OTUs) across 223 heterogeneous terrestrial, aquatic and phyllosphere bacterial assemblages. Taxa were considered potential seeds if they transitioned from rare to abundant somewhere within the metacommunity and if they were ubiquitous and able to persist under unfavorable conditions, the latter assessed by checking their presence in three deeply sequenced samples (one soil, one river and one lake, 2.2-3 million reads per sample). We show that only a small fraction (13%) of all detected OTUs constitute a metacommunity seed bank that is shared between all terrestrial and aquatic communities, but not by phyllosphere assemblages, which seem to recruit from a different taxa pool. Our results suggest directional recruitment driven by the flow of water in the landscape, since most aquatic sequences were associated to OTUs found in a single deeply-sequenced soil sample, but only 45% of terrestrial sequences belonged to OTUs found in the two deeply-sequenced aquatic communities. Finally, we hypothesize that extreme rarity, and its interplay with water residence time and growth rates, may further constrain the size of the potential seed bank.

Exploring the Ecological Coherence between the Spatial and Temporal Patterns of Bacterioplankton in Boreal Lakes.

One of the major contemporary challenges in microbial ecology has been to discriminate the reactive core from the random, unreactive components of bacterial communities. In previous work we used the spatial abundance distributions of bacterioplankton across boreal lakes of Québec to group taxa into four distinct categories that reflect either hydrology-mediated dispersal along the aquatic network or environmental selection mechanisms within lakes. Here, we test whether this categorization derived from the spatial distribution of taxa is maintained over time, by analyzing the temporal dynamics of the operational taxonomic units (OTUs) within those spatially derived categories along an annual cycle in the oligotrophic lake Croche (Québec, Canada), and assessing the coherence in the patterns of abundance, occurrence, and environmental range of these OTUs over space and time. We report that the temporal dynamics of most taxa within a single lake are largely coherent with those derived from their spatial distribution over large spatial scales, suggesting that these properties must be intrinsic of particular taxa. We also identified a set of rare taxa cataloged as having a random occupancy based on their spatial distribution, but which showed clear seasonality and abundance peaks along the year, yet these comprised a very small fraction of the total rare OTUs. We conclude that the presence of most rare bacterioplankton taxa in boreal lakes is random, since both their temporal and spatial dynamics suggest links to passive downstream transport and persistence in freshwater networks, rather than environmental selection.

Terrestrial support of lake food webs: Synthesis reveals controls over cross-ecosystem resource use.

Widespread evidence that organic matter exported from terrestrial into aquatic ecosystems supports recipient food webs remains controversial. A pressing question is not only whether high terrestrial support is possible but also what the general conditions are under which it arises. We assemble the largest data set, to date, of the isotopic composition (δ2H, δ13C, and δ15N) of lake zooplankton and the resources at the base of their associated food webs. In total, our data set spans 559 observations across 147 lakes from the boreal to subtropics. By predicting terrestrial resource support from within-lake and catchment-level characteristics, we found that half of all consumer observations that is, the median were composed of at least 42% terrestrially derived material. In general, terrestrial support of zooplankton was greatest in lakes with large physical and hydrological connections to catchments that were rich in aboveground and belowground organic matter. However, some consumers responded less strongly to terrestrial resources where within-lake production was elevated. Our study shows that multiple mechanisms drive widespread cross-ecosystem support of aquatic consumers across Northern Hemisphere lakes and suggests that changes in terrestrial landscapes will influence ecosystem processes well beyond their boundaries.

Transport and transformation of soil-derived CO2, CH4 and DOC sustain CO2 supersaturation in small boreal streams.

Streams are typically supersaturated in carbon dioxide (CO2) and methane (CH4), and are recognized as important components of regional carbon (C) emissions in northern landscapes. Whereas there is consensus that in most of the systems the CO2 emitted by streams represents C fixed in the terrestrial ecosystem, the pathways delivering this C to streams are still not well understood. We assessed the contribution of direct soil CO2 injection versus the oxidation of soil-derived dissolved organic C (DOC) and CH4 in supporting CO2 supersaturation in boreal streams in Québec. We measured the concentrations of CO2, CH4 and DOC in 43 streams and adjacent soil waters during summer base-flow period. A mass balance approach revealed that all three pathways are significant, and that the mineralization of soil-derived DOC and CH4 accounted for most of the estimated stream CO2 emissions (average 75% and 10%, respectively), and that these estimated contributions did not change significantly between the studied low order (≤3) streams. Whereas some of these transformations take place in the channel proper, our results suggest that they mainly occur in the hyporheic zones of the streams. Our results further show that stream CH4 emissions can be fully explained by soil CH4 inputs. This study confirms that these boreal streams, and in particular their hyporheic zones, are extremely active processors of soil derived DOC and CH4, not just vents for soil produced CO2.

Landscape-scale spatial abundance distributions discriminate core from random components of boreal lake bacterioplankton.

Aquatic bacterial communities harbour thousands of coexisting taxa. To meet the challenge of discriminating between a 'core' and a sporadically occurring 'random' component of these communities, we explored the spatial abundance distribution of individual bacterioplankton taxa across 198 boreal lakes and their associated fluvial networks (188 rivers). We found that all taxa could be grouped into four distinct categories based on model statistical distributions (normal like, bimodal, logistic and lognormal). The distribution patterns across lakes and their associated river networks showed that lake communities are composed of a core of taxa whose distribution appears to be linked to in-lake environmental sorting (normal-like and bimodal categories), and a large fraction of mostly rare bacteria (94% of all taxa) whose presence appears to be largely random and linked to downstream transport in aquatic networks (logistic and lognormal categories). These rare taxa are thus likely to reflect species sorting at upstream locations, providing a perspective of the conditions prevailing in entire aquatic networks rather than only in lakes.