Multisubstrate DNA stable isotope probing reveals guild structure of bacteria that mediate soil carbon cycling

Soil microorganisms determine the fate of soil organic matter (SOM), and their activities compose a major component of the global carbon (C) cycle. We employed a multisubstrate, DNA-stable isotope probing experiment to track bacterial assimilation of C derived from distinct sources that varied in bioavailability. This approach allowed us to measure microbial contributions to SOM processing by measuring the C assimilation dynamics of diverse microorganisms as they interacted within soil. We identified and tracked 1,286 bacterial taxa that assimilated 13C in an agricultural soil over a period of 48 d. Overall 13C-assimilation dynamics of bacterial taxa, defined by the source and timing of the 13C they assimilated, exhibited low phylogenetic conservation. We identified bacterial guilds composed of taxa that had similar 13C assimilation dynamics. We show that C-source bioavailability explained significant variation in both C mineralization dynamics and guild structure, and that the growth dynamics of bacterial guilds differed significantly in response to C addition. We also demonstrate that the guild structure explains significant variation in the biogeographical distribution of bacteria at continental and global scales. These results suggest that an understanding of in situ growth dynamics is essential for understanding microbial contributions to soil C cycling. We interpret these findings in the context of bacterial life history strategies and their relationship to terrestrial C cycling.

Different impacts of an electron shuttle on nitrate- and nitrite-dependent anaerobic oxidation of methane in paddy soil

Quinones, redox-active functional groups in soil organic matter, can act as electron shuttles for microbial anaerobic transformation. Here, we used ¹³CH₄ to trace ¹³C conversion (¹³C-CO₂ + ¹³C-SOC) to investigate the influence of an artificial electron shuttle (anthraquinone-2,6-disulfonate, AQDS) on denitrifying anaerobic methane oxidation (DAMO) in paddy soil. The results showed that AQDS could act as the terminal electron acceptor for the anaerobic oxidation of methane (AOM) in the paddy field. Moreover, AQDS significantly enhanced nitrate-dependent AOM rates and the amount of ¹³C-CH₄ assimilation to soil organic carbon (SOC), whereas it was remarkably reduced nitrite-dependent AOM rates and ¹³C assimilation. Ultimately, AQDS notably increased the total DAMO rates and ¹³C assimilation to SOC. However, the electron shuttle did not change the percentage of ¹³C-SOC in total ¹³C-CH₄ conversion. These results suggest that electron shuttles in the natural organic matter might be able to offset methane emission by facilitating AOM coupled with the denitrification process.

Life history strategies explain bacterial activity in the soil carbon cycle

Soil microorganisms determine the fate of soil organic matter (SOM), and their activities comprise a major component of the global carbon (C) cycle. We sought to comprehend the physiological and ecological mechanisms underpinning microbial contributions to SOM dynamics by examining the activities of individual microorganisms within a complex soil system. We determined bacterial activity by using a multi-substrate DNA-stable isotope probing experiment to track C assimilation dynamics across thousands of bacteria within an agricultural soil. In this way, we identified 1,286 bacterial taxa assimilating C from SOM. Substrate bioavailability explained significant variation in mineralization rates and microbial assimilation dynamics. We show that, while patterns of C assimilation exhibited little phylogenetic conservation above the species level, these patterns defined functional clusters whose properties exemplified broad differences in life history strategy, particularly along the copiotroph-oligotroph continuum. We also show that these functional clusters explain soil community response to fresh litter, and patterns of microbial biogeography at continental and global scales. Our results add to the growing body of knowledge indicating that life history theory provides a useful framework for understanding microbial contributions to terrestrial C-cycling.

Leaf Photosynthesis and Carbon Metabolism Adapt to Crop Load in ‘Gala’ Apple Trees

It is widely accepted that a tight coordination between carbon (C) utilization in the sink and C assimilation and metabolism in the source exists in higher plants. However, much of our current understanding is based on research from herbaceous plants, where the source and sink interaction is less sophisticated compared to woody perennials with a significant sink presence. Apple (Malus x domestica Borkh.) is a good representative of the latter category, and its production and transport of sorbitol, in addition to sucrose, adds complexity to C regulation. In this study, four-year-old “Gala”/”M.26” apple trees were subjected to crop load levels at 2.5, 7.5, and 15 fruits/cm2 trunk cross-sectional area. Low crop load trees exhibited reduced leaf C assimilation and extra accumulation of non-structural carbohydrates (NSC). This was primarily a result of reduced activity of Rubisco and increased activities of key enzymes that synthesize starch, sucrose, and sorbitol. Among the NSC, leaf starch was found to be most sensitive to crop load and could function as a leading indicator for source–sink balance in apple. However, even the high crop load trees still retained a significant amount of NSC in leaves at dawn, demonstrating that apple is fundamentally different from herbaceous plants in the way it balances leaf carbon inventories at dawn with carbon export at night for sink growth.

Leaf Nitrogen Traits in Response to Plant Density and Nitrogen Supply in Oilseed Rape

Understanding the response of plant nitrogen (N) and carbon (C) economies in oilseed rape, as well as their role in defining phenotypic plasticity, is necessary for designing new strategies to optimize plant and canopy C assimilation to improve potential yield. This paper aims to elucidate the extent to which the interaction between N supply and plant population density alters N distribution in oilseed rape plant (Brassica napus L.) and whether this interaction changes plant investment in leaf area or leaf mass per area. Spring oilseed rape was grown at two rates of N supply (50 and 150 kg N·ha−1) and two plant population densities (50 and 150 plants·m−2). Photosynthesis, leaf area, leaf biomass, and N content of selected leaves were measured at 20% of flowers on main raceme open. The interaction between N supply and plant population density altered leaf N content per area, which is the main determinant of photosynthesis. This interaction also affected leaf mass per area, while N supply determined N content per unit leaf mass. These results suggest that the interaction between N supply and population density affects both nitrogen distribution and leaf mass per area, which could have important implications for light distribution and, therefore, for C assimilation at the plant level.

Carbon assimilation through a vertical light gradient in the canopy of invasive herbs grown under different temperature regimes is determined by leaf and whole-plant architecture

This study examined the acclimation to temperature of two globally invasive species Iris pseudacorus and Lythrum salicaria, which share the same habitat type but differ in morphology. Iris pseudacorus has long vertical leaves, allowing light penetration through the canopy, while L. salicaria has stems with small horizontal leaves, creating significant self-shading. We aimed to build a physiological understanding of how these two species respond to different growth temperatures with regard to growth and gas exchange-related traits over the canopy. Growth and gas exchange-related traits in response to low (15 °C) and high (25 °C) growth temperature regimes were compared. Plants were grown in growth chambers, and light response curves were measured with infrared gas analysers after 23–33 days at three leaf positions on each plant, following the vertical light gradient through the canopy. After 37 days of growth, above-ground biomass, photosynthetic pigments and leaf N concentration were determined. The maximum photosynthesis rate was lower in lower leaf positions but did not differ significantly between temperatures. Iris pseudacorus photosynthesis decreased with decreasing leaf position, more so than L. salicaria. This was explained by decreasing N and chlorophyll concentrations towards the leaf base in I. pseudacorus, while pigment concentrations increased towards the lower canopy in L. salicaria. Biomass, shoot height and specific leaf area increased with temperature, more so in I. pseudacorus than in L. salicaria. Light response curves revealed that L. salicaria had a higher degree of shade acclimation than I. pseudacorus, probably due to self-shading in L. salicaria. High temperature decreased C assimilation at the bottom of the canopy in L. salicaria, while C assimilation in I. pseudacorus was less affected by temperature. As vegetative growth and flowering was stimulated by temperature, the invasive potential of these species is predicted to increase under global warming.

Nutrient Source and Mycorrhizal Association jointly alters Soil Microbial Communities that shape Plant-Rhizosphere-Soil Carbon-Nutrient Flows

Interactions between plants and microorganisms strongly affect ecosystem functioning as processes of plant productivity, litter decomposition and nutrient cycling are controlled by both organisms. Though two-sided interactions between plants and microorganisms and between microorganisms and litter decomposition are areas of major scientific research, our understanding of the three-sided interactions of plant-derived carbon flow into the soil microbial community and their follow-on effects on ecosystem processes like litter decomposition and plant nutrient uptake remains limited. Therefore, we performed a greenhouse experiment with two plant communities differing in their ability to associate with arbuscular mycorrhizal fungi (AMF). By applying a 13CO2 pulse label to the plant communities and adding various 15N labelled substrate types to ingrowth cores, we simultaneously traced the flow of plant-derived carbon into soil microbial communities and the return of mineralized nitrogen back to the plant communities. We observed that net 13C assimilation by the rhizosphere microbial communities and their community composition not only depended on plant-AMF association but also type of substrate being decomposed. AMF-association resulted in lower net 13C investment into the decomposer community than absence of the association for similar 15N uptake. This effect was driven by a reduced carbon flow to fungal and bacterial saprotrophs and a simultaneous increase of carbon flow to AMF. Additionally, in presence of AMF association CN flux also depended on the type of substrate being decomposed. Lower net 13C assimilation was observed for decomposition of plant-derived and microorganism-derived substrates whereas opposite was true for inorganic nitrogen. Interestingly, the decomposer communities assembled in the rhizosphere were structured by both the plant community and substrate amendments which suggests existence of functional overlap between the two soil contexts. Moreover, we present preliminary evidence that AMF association helps plants access nutrients that are locked in bacterial and plant necromass at a lower carbon cost. Therefore, we conclude that a better understanding of ecosystem processes like decomposition can only be achieved when the whole plant-microorganism-litter context is investigated.

No carbon limitation after lower crown loss in Pinus radiata

Background and Aims Biotic and abiotic stressors can cause different defoliation patterns within trees. Foliar pathogens of conifers commonly prefer older needles and infection with defoliation that progresses from the bottom crown to the top. The functional role of the lower crown of trees is a key question to address the impact of defoliation caused by foliar pathogens. Methods A 2 year artificial defoliation experiment was performed using two genotypes of grafted Pinus radiata to investigate the effects of lower-crown defoliation on carbon (C) assimilation and allocation. Grafts received one of the following treatments in consecutive years: control–control, control–defoliated, defoliated–control and defoliated–defoliated. Results No upregulation of photosynthesis either biochemically or through stomatal control was observed in response to defoliation. The root:shoot ratio and leaf mass were not affected by any treatment, suggesting prioritization of crown regrowth following defoliation. In genotype B, defoliation appeared to impose C shortage and caused reduced above-ground growth and sugar storage in roots, while in genotype A, neither growth nor storage was altered. Root C storage in genotype B decreased only transiently and recovered over the second growing season. Conclusions In genotype A, the contribution of the lower crown to the whole-tree C uptake appears to be negligible, presumably conferring resilience to foliar pathogens affecting the lower crown. Our results suggest that there is no C limitation after lower-crown defoliation in P. radiata grafts. Further, our findings imply genotype-specific defoliation tolerance in P. radiata.

Non-structural carbohydrate pools not linked to hydraulic strategies or carbon supply in tree saplings during severe drought and subsequent recovery

Non-structural carbohydrate (NSC) pools fluctuate based on the interplay between photosynthesis, demand from various carbon (C) sinks and tree hydraulic status. Thus, it has been hypothesized that tree species with isohydric stomatal control (i.e., trees that close stomata rapidly in response to drought) rely heavily on NSC pools to sustain metabolism, which can lead to negative physiological consequences such as C depletion. Here, we seek to use a species’ degree of isohydry or anisohydry as a conceptual framework for understanding the interrelations between photosynthetic C supply, hydraulic damage and fluctuations in NSC pools. We conducted a 6-week experimental drought, followed by a 6-week recovery period, in a greenhouse on seven tree species that span the spectrum from isohydric to anisohydric. Throughout the experiment, we measured photosynthesis, hydraulic damage and NSC pools. Non-structural carbohydrate pools were remarkably stable across species and tissues—even highly isohydric species that drastically reduced C assimilation were able to maintain stored C. Despite these static NSC pools, we still inferred an important role for stored C during drought, as most species converted starches into sugars during water stress (and back again post-drought). Finally, we did not observe any linkages between C supply, hydraulic damage and NSC pools, indicating that NSC was maintained independent of variation in photosynthesis and hydraulic function. Our results advance the idea that C depletion is a rare phenomenon due to either active maintenance of NSC pools or sink limitation, and thus question the hypothesis that reductions in C assimilation necessarily lead to C depletion.