Simulated rhizosphere deposits induce microbial N-mining that may accelerate shrubification in the subarctic

Climate change is exposing high-latitude systems to warming and a shift towards more shrub-dominated plant communities, resulting in increased leaf-litter inputs at the soil surface, and more labile root-derived organic matter (OM) input in the soil profile. Labile OM can stimulate the mineralization of soil organic matter (SOM); a phenomenon termed “priming.” In N-poor subarctic soils, it is hypothesized that microorganisms may “prime” SOM in order to acquire N (microbial N-mining). Increased leaf-litter inputs with a high C/N ratio might further exacerbate microbial N demand, and increase the susceptibility of N-poor soils to N-mining. We investigated the N-control of SOM mineralization by amending soils from climate change–simulation treatments in the subarctic (+1.1°C warming, birch litter addition, willow litter addition, and fungal sporocarp addition) with labile OM either in the form of glucose (labile C; equivalent to 400 µg C/g fresh [fwt] soil) or alanine (labile C + N; equivalent to 400 µg C and 157 µg N/g fwt soil), to simulate rhizosphere inputs. Surprisingly, we found that despite 5 yr of simulated climate change treatments, there were no significant effects of the field-treatments on microbial process rates, community structure or responses to labile OM. Glucose primed the mineralization of both C and N from SOM, but gross mineralization of N was stimulated more than that of C, suggesting that microbial SOM use increased in magnitude and shifted to components richer in N (i.e., selective microbial N-mining). The addition of alanine also resulted in priming of both C and N mineralization, but the N mineralization stimulated by alanine was greater than that stimulated by glucose, indicating strong N-mining even when a source of labile OM including N was supplied. Microbial carbon use efficiency was reduced in response to both labile OM inputs. Overall, these findings suggest that shrub expansion could fundamentally alter biogeochemical cycling in the subarctic, yielding more N available for plant uptake in these N-limited soils, thus driving positive plant–soil feedbacks

Nutrient limitations to bacterial and fungal growth during cellulose decomposition in tropical forest soils

Nutrients constrain the soil carbon cycle in tropical forests, but we lack knowledge on how these constraints vary within the soil microbial community. Here, we used in situ fertilization in a montane tropical forest and in two lowland tropical forests on contrasting soil types to test the principal hypothesis that there are different nutrient constraints to different groups of microorganisms during the decomposition of cellulose. We also tested the hypotheses that decomposers shift from nitrogen to phosphorus constraints from montane to lowland forests, respectively, and are further constrained by potassium and sodium deficiency in the western Amazon. Cellulose and nutrients (nitrogen, phosphorus, potassium, sodium, and combined) were added to soils in situ, and microbial growth on cellulose (phospholipid fatty acids and ergosterol) and respiration were measured. Microbial growth on cellulose after single nutrient additions was highest following nitrogen addition for fungi, suggesting nitrogen as the primary limiting nutrient for cellulose decomposition. This was observed at all sites, with no clear shift in nutrient constraints to decomposition between lowland and montane sites. We also observed positive respiration and fungal growth responses to sodium and potassium addition at one of the lowland sites. However, when phosphorus was added, and especially when added in combination with other nutrients, bacterial growth was highest, suggesting that bacteria out-compete fungi for nitrogen where phosphorus is abundant. In summary, nitrogen constrains fungal growth and cellulose decomposition in both lowland and montane tropical forest soils, but additional nutrients may also be of critical importance in determining the balance between fungal and bacterial decomposition of cellulose.This study is a product of the Andes Biodiversity and Ecosystem Research Group consortium (www.andesconservation.org) and was financed by the UK Natural Environment Research Council NE/G018278/1 to PM, a European Union Marie-Curie Fellowship FP7-2012-329360 to ATN and ARC award DP170104091 to PM

Pathways from research to sustainable development: insights from ten research projects in sustainability and resilience

Drawing on collective experience from ten collaborative research projects focused on the Global South, we identify three major challenges that impede the translation of research on sustainability and resilience into better-informed choices by individuals and policy-makers that in turn can support transformation to a sustainable future. The three challenges comprise: (i) converting knowledge produced during research projects into successful knowledge application; (ii) scaling up knowledge in time when research projects are short-term and potential impacts are long-term; and (iii) scaling up knowledge across space, from local research sites to larger-scale or even global impact. Some potential pathways for funding agencies to overcome these challenges include providing targeted prolonged funding for dissemination and outreach, and facilitating collaboration and coordination across different sites, research teams, and partner organizations. By systematically documenting these challenges, we hope to pave the way for further innovations in the research cycle

Controls on carbon cycling in tropical soils from the Amazon to the Andes: the influence of climate, plant inputs, nutrients and soil organisms

Tropical soils are a globally important store of terrestrial carbon (C) and source of atmospheric carbon dioxide (CO2), regulated by the activity of soil microorganisms, through the mineralisation of plant residues and soil organic matter (SOM). Climatic warming will influence microbial activity, and this may accelerate the rate of C release from soils as CO2, contributing to alterations in current atmospheric composition, and generating feedbacks to climate change. Yet the magnitude of C loss from tropical soils remains uncertain, partly because we do not fully understand how non-climatic factors – including the chemistry of plant inputs, the availability of soil nutrients and the composition of the decomposer community – will interact to determine the response to changes in temperature. This thesis examines how these factors together regulate the rate of C cycling in contrasting soils across a 3400 m tropical elevation gradient in the Peruvian Andes, spanning a 20 ºC range (6.5 – 26.4 ºC) in mean annual temperature. Large-scale field-based manipulation experiments, translocating leaves and soil-cores across the elevation gradient (to impose an in-situ experimental warming treatment), were combined with controlled laboratory studies to examine the microbial-scale mechanisms which underlie the processes of decomposition and soil respiration observed in-situ. Results show that, across the gradient, rates of leaf-decomposition were determined principally by temperature and foliar chemical traits, while soil fertility had no significant influence. The effect of temperature was, however, stronger across higher-elevation sites, suggesting a greater vulnerability of the C-rich soils in montane systems to increased C loss under climatic warming. In lowland forests, the presence of invertebrate macrofauna also accelerated rates of decomposition, but leaf chemistry explained the greatest proportion of the observed variance, with a strong role for leaf chemical traits also identified under controlled conditions. Despite marked differences in microbial abundance and community composition among soils, these metrics were not associated with observed rates of decomposition. These results suggest that climate-related changes to plant species distributions (with associated changes to the chemistry of leaf-inputs), and upslope extension of macrofaunal ranges, could strongly influence future rates of leaf decomposition, independently of the direct response to warming. From the soil translocation study, root-soil interactions stimulated substantial net C loss from montane soils following translocation downslope (experimental warming treatment), indicating that warming-related changes to root productivity, exudation and/or species-composition could represent an important mode of future C loss from these soils. To examine more closely how inputs of plant-derived C influence the turnover of pre-existing SOM, and whether soil nutrient availability modulates the response, soils were amended with simple and complex 13C-labelled substrates in combination with inorganic nutrient treatments. Isotopic partitioning was used to determine the degree to which C and nutrient inputs accelerated (positive priming) or retarded (negative priming) the decomposition of SOM. Amendment of upper montane forest and montane grassland soils with nitrogen (N; alone and in combination with C) substantially retarded the decomposition of SOM, suggesting that microbial demand for N strongly regulates the turnover of organic matter in these soils. In contrast, amendment of lower montane and lowland forest soils with C stimulated positive priming of SOM, which was strongest in response to the simple C substrate and was not influenced by nutrient treatments, suggesting that microorganisms in these soils are primarily constrained by availability of labile C. Functional differences among microbial groups were also evident, with gram-negative bacteria and fungi using more labile sources of C while gram-positive bacteria used more complex C. Together, results from these studies considerably advance our understanding of soil C dynamics across lowland and montane systems, painting a rich picture of interacting processes which will determine the future soil C balance in tropical ecosystems. They show that the influence of temperature on the rate of soil C cycling is strongly affected by the nature and composition of plant-derived and atmospheric inputs, the principal additional constraints varying with elevation, leading to both opposing and reinforcing effects on rates of decomposition. The greater observed temperature sensitivity of decomposition at higher elevations is coupled with high microbial demand for N which regulates the turnover of SOM, whereas at lower elevations leaf decomposition is accelerated by active macrofaunal breakdown, while microbial decomposition of SOM is constrained by the availability of labile C. Under a global change scenario of increased temperature and N deposition, results therefore suggest that: (i) modified chemistry of plant inputs will influence rates of decomposition, independently of climate; (ii) increased availability of labile C will lead to more rapid decomposition of SOM at lower elevations; (iii) greater root productivity (associated with warming and plant-community shifts) will stimulate soil C loss across montane regions; but (iv) at higher elevations, a possible countervailing effect may be imposed on rapid warming-accelerated decomposition if increased N availability reduces microbial mineralisation of SOM. The net effect on the ecosystem C budget will depend on the balance of C gain from primary productivity and C loss from soils. Overall, however, the results presented here suggest that the large soil C stores in higher-elevation montane regions are particularly vulnerable to substantial reductions under exposure to short- and medium-term climatic warming

Microbial resilience to drying-rewetting is partly driven by selection for quick colonizers

Rewetting dry soil induces enormous changes in microbial growth and biogeochemistry. Upon drying-rewetting (D/RW), bacteria have been shown to exhibit two different responses: (1) a more resilient response where bacteria start growing immediately with a quick recovery after rewetting and (2) a less resilient response where there is a pronounced lag-period before bacterial growth starts to increase exponentially. A shift towards a more resilient bacterial growth response has previously been shown to be induced by exposing soils to repeated cycles of D/RW. Here, we test the hypothesis that this response is driven by selection for a bacterial community with traits for quick colonization of labile carbon (C) resources made available upon D/RW. To do so, we compared the responses of soils that had been exposed to either (i) three cycles of D/RW, (ii) three pulses of glucose addition to moist soil or (iii) three pulses of litter addition to moist soil, before all soils were subjected to a D/RW event where bacterial growth, fungal growth and respiration rates were monitored. As expected, exposing the soil to a series of D/RW events resulted in a more resilient bacterial growth response, as well as a faster recovery of fungal growth. Pre-treating the soils with pulses of glucose accelerated the recovery of bacteria after D/RW, but did not select for a bacterial resilience that could match the pre-treatment with exposure to D/RW. Pre-treatment with pulses of litter showed a trend for an accelerated recovery of bacterial growth to D/RW, but to a lesser extent than that induced by pulses of glucose. In contrast, pre-treatment of soil with either pulses of glucose or pulses of litter both led to a faster recovery of fungal growth following D/RW, matching that induced by repeated D/RW cycles. These results suggest that selection for quick colonizers partly explains the shift to a more resilient microbial response to repeated cycles of D/RW, accounting for ca. 60% increase in bacterial resilience and 100% of the increase in fungal resilience compared that induced by repeated D/RW cycles

Nutrient limitation may induce microbial mining for resources from persistent soil organic matter

Fungi and bacteria are the two principal microbial groups in soil, responsible for the breakdown of organic matter (OM). The relative contribution of fungi and bacteria to decomposition is thought to impact biogeochemical cycling at the ecosystem scale, whereby bacterially dominated decomposition supports the fast turnover of easily available substrates, whereas fungal-dominated decomposition leads to the slower turnover of more complex OM. However, empirical support for this is lacking. We used soils from a detritus input and removal treatment experiment in an old-growth coniferous forest, where above- and belowground litter inputs have been manipulated for 20 yr. These manipulations have generated variation in OM quality, as defined by energetic content and proxied as respiration per g soil organic matter (SOM) and the δ13C signature in respired CO2 and microbial PLFAs. Respiration per g SOM reflects the availability and lability of C substrate to microorganisms, and the δ13C signature indicates whether the C used by microorganisms is plant derived and higher quality (more δ13C depleted) or more microbially processed and lower quality (more δ13C enriched). Surprisingly, higher quality C did not disproportionately benefit bacterial decomposers. Both fungal and bacterial growth increased with C quality, with no systematic change in the fungal-to-bacterial growth ratio, reflecting the relative contribution of fungi and bacteria to decomposition. There was also no difference in the quality of C targeted by bacterial and fungal decomposers either for catabolism or anabolism. Interestingly, respired CO2 was more δ13C enriched than soil C, suggesting preferential use of more microbially processed C, despite its lower quality. Gross N mineralization and consumption were also unaffected by differences in the ratio of fungal-to-bacterial growth. However, the ratio of C to gross N mineralization was lower than the average C/N of SOM, meaning that microorganisms specifically targeted N-rich components of OM, indicative of selective microbial N-mining. Consistent with the δ13C data, this reinforces evidence for the use of more microbially processed OM with a lower C/N ratio, rather than plant-derived OM. These results challenge the widely held assumption that microorganisms favor high-quality C sources and suggest that there is a trade-off in OM use that may be related to the growth-limiting factor for microorganisms in the ecosystem

Will a legacy of enhanced resource availability accelerate the soil microbial response to future climate change?

Soil microorganisms play an integral role in the regulation of carbon (C) cycling. In high-latitude ecosystems, climate warming is leading to higher plant productivity, shrub expansion and faster nutrient cycling; all of which increase resource availability to soil microorganisms. To understand how a legacy of enhanced resource availability affects the functional traits of microbial communities, and their feedbacks to further environment change, we collected soils from a field-experiment in a subarctic dry heath, where the consequences of climate warming were simulated by adding birch litter or inorganic N as either chronic additions during three years or as a single extreme addition. Soils were then re-exposed to the same resource or a modified resource environment in the laboratory and were monitored for 2 months. We hypothesized that a history of resource input would affect microbial functional profiles, which could result in two possibilities: 1) soil microbes exposed to a historical resource input would perform better when presented with the same resource, because the communities would be specialized to use the added resource, or 2) soil microbes would perform better when presented with a new resource, because the added resource would relieve the nutrient limitation induced by the previous resource input. We also hypothesized that with the same resource, a chronic and long-term input (i.e., a press disturbance) would select for K-strategists (i.e., fungi), while a sudden and large input (i.e., a pulse disturbance) would select for r-strategists (i.e., bacteria). We observed that bacteria in soils exposed to a history of N input showed a stronger growth response to new litter addition, while fungi in soils with a history of litter input showed a stronger growth response to both new litter and new N additions. When presented with new litter, the increase of fungal growth in soil from the extreme litter field-treatment was lower than in the chronic litter field-treatment, demonstrating that a pulse disturbance could weaken the stimulation of fungal growth. When presented with new litter, the increases of bacterial growth did not differ between the chronic N field-treatment and the extreme N field-treatment, suggesting that bacterial responses were not favoured by a press disturbance. We conclude that the enhanced resource availabilities expected in warming arctic soils will generate a positive microbial feedback to climate change