Soil organic carbon stocks in estuarine and marine mangrove ecosystems are driven by nutrient colimitation of P and N

Mangroves play an important role in carbon sequestration, but soil organic carbon (SOC) stocks differ between marine and estuarine mangroves, suggesting differing processes and drivers of SOC accumulation. Here, we compared undegraded and degraded marine and estuarine mangroves in a regional approach across the Indonesian archipelago for their SOC stocks and evaluated possible drivers imposed by nutrient limitations along the land‐to‐sea gradients. SOC stocks in natural marine mangroves (271–572 Mg ha^?1 m^?1) were much higher than under estuarine mangroves (100–315 Mg ha^?1 m^?1) with a further decrease caused by degradation to 80–132 Mg ha^?1 m^?1. Soils differed in C/N ratio (marine: 29–64; estuarine: 9–28), δ¹⁵N (marine: ?0.6 to 0.7‰; estuarine: 2.5 to 7.2‰), and plant‐available P (marine: 2.3–6.3 mg kg^?1; estuarine: 0.16–1.8 mg kg^?1). We found N and P supply of sea‐oriented mangroves primarily met by dominating symbiotic N₂ fixation from air and P import from sea, while mangroves on the landward gradient increasingly covered their demand in N and P from allochthonous sources and SOM recycling. Pioneer plants favored by degradation further increased nutrient recycling from soil resulting in smaller SOC stocks in the topsoil. These processes explained the differences in SOC stocks along the land‐to‐sea gradient in each mangrove type as well as the SOC stock differences observed between estuarine and marine mangrove ecosystems. This first large‐scale evaluation of drivers of SOC stocks under mangroves thus suggests a continuum in mangrove functioning across scales and ecotypes and additionally provides viable proxies for carbon stock estimations in PES or REDD schemes.     

Small scale variability of vertical water and dissolved organic matter fluxes in sandy Cambisol subsoils as revealed by segmented suction plates

Dissolved organic matter (DOM) is considered as a major carbon source in subsoils. As soil water fluxes are highly variable at small scale, and transport versus sorptive retention of DOM is related to water flux and associated contact time with minerals, knowledge of the small scale spatial variability of the dissolved organic carbon (DOC) concentrations and fluxes into the subsoil is decisive for a solid estimation of organic carbon (OC) translocation into the subsoil. Here, we made advantage of novel segmented suction plates (4 × 4 segments, each 36 cm²) to analyze the small scale spatial and temporal variability of DOC transport at 10, 50 and 150 cm depth of three subsoil observatories (approximately 50 m apart) in a sandy Dystric Cambisol under beech in the Grinderwald, 40 km northwest from Hannover, Germany. Water fluxes, DOC concentrations and fluxes as well as the specific UV absorbance (SUVA) at 280 nm were determined in weekly samples from August 2014 to November 2015 for each individual segment. The DOC fluxes decreased with depth (19.6 g C m^?2 year^?1, 10 cm; 1.2 g C m^?2 year^?1, 150 cm) and were strongly related to the water fluxes. The SUVA at 280 nm also decreased with depth (0.03 L mg C^?1 cm^?1, 10 cm; 0.01 L mg C^?1 cm^?1, 150 cm), indicating a selective retention of aromatic moieties, that was eased with increasing water flux at least in the subsoil. The proportion of temporal fluctuations and small scale variability on the total variance of each parameter where determined by the calculation of intra class correlations. The seasonal heterogeneity and the small scale spatial heterogeneity were identified to be of major importance. The importance of the small scale spatial heterogeneity strongly increased with depth, pointing towards the stability of flow paths and suggesting that at a given substrate hydrological processes rather than physicochemical processes are decisive for the sorptive retention of DOM and the variability of OC accumulation in the subsoil. Our results clearly show the demand of small scale sampling for the identification of processes regarding carbon cycling in the subsoil.     

Neuron navigator 3a regulates liver organogenesis during zebrafish embryogenesis

Endodermal organogenesis requires a precise orchestration of cell fate specification and cell movements, collectively coordinating organ size and shape. In Caenorhabditis elegans, uncoordinated-53 (unc-53) encodes a neural guidance molecule that directs axonal growth. One of the vertebrate homologs of unc-53 is neuron navigator 3 (Nav3). Here, we identified a novel vertebrate neuron navigator 3 isoform in zebrafish, nav3a, and we provide genetic evidence in loss- and gain-of-function experiments showing its functional role in endodermal organogenesis during zebrafish embryogenesis. In zebrafish embryos, nav3a expression was initiated at 22 hpf in the gut endoderm and at 40 hpf expanded to the newly formed liver bud. Endodermal nav3a expression was controlled by Wnt2bb signaling and was independent of FGF and BMP signaling. Morpholino-mediated knockdown of nav3a resulted in a significantly reduced liver size, and impaired development of pancreas and swim bladder. In vivo time-lapse imaging of liver development in nav3a morphants revealed a failure of hepatoblast movement out from the gut endoderm during the liver budding stage, with hepatoblasts being retained in the intestinal endoderm. In hepatocytes in vitro, nav3a acts as a positive modulator of actin assembly in lamellipodia and filipodia extensions, allowing cellular movement. Knockdown of nav3a in vitro impeded hepatocyte movement. Endodermal-specific overexpression of nav3a in vivo resulted in additional ectopic endodermal budding beyond the normal liver and pancreatic budding sites. We conclude that nav3a is required for directing endodermal organogenesis involving coordination of endodermal cell behavior.     

Stabilization of Soil Organic Matter: Association with Minerals or Chemical Recalcitrance?

Soil organic matter (OM) can be stabilized against decomposition by association with minerals, by its inherent recalcitrance and by occlusion in aggregates. However, the relative contribution of these factors to OM stabilization is yet unknown. We analyzed pool size and isotopic composition (¹⁴C, ¹³C) of mineral-protected and recalcitrant OM in 12 subsurface horizons from 10 acidic forest soils. The results were related to properties of the mineral phase and to OM composition as revealed by CPMAS ¹³C-NMR and CuO oxidation. Stable OM was defined as that material which survived treatment of soils with 6 wt% sodium hypochlorite (NaOCl). Mineral-protected OM was extracted by subsequent dissolution of minerals by 10% hydrofluoric acid (HF). Organic matter resistant against NaOCl and insoluble in HF was considered as recalcitrant OM. Hypochlorite removed primarily ¹⁴C-modern OM. Of the stable organic carbon (OC), amounting to 2.4–20.6 g kg⁻¹ soil, mineral dissolution released on average 73%. Poorly crystalline Fe and Al phases (Fe_o, Al_o) and crystalline Fe oxides (Fe_d−o) explained 86% of the variability of mineral-protected OC. Atomic C_p/(Fe+Al)_p ratios of 1.3–6.5 suggest that a portion of stable OM was associated with polymeric Fe and Al species. Recalcitrant OC (0.4–6.5 g kg⁻¹ soil) contributed on average 27% to stable OC and the amount was not correlated with any mineralogical property. Recalcitrant OC had lower Δ¹⁴C and δ¹³C values than mineral-protected OC and was mainly composed of aliphatic (56%) and O-alkyl (13%) C moieties. Lignin phenols were only present in small amounts in either mineral-protected or recalcitrant OM (mean 4.3 and 0.2 g kg⁻¹ OC). The results confirm that stabilization of OM by interaction with poorly crystalline minerals and polymeric metal species is the most important mechanism for preservation of OM in these acid subsoil horizons.     

Fate and stability of dissolved organic carbon in topsoils and subsoils under beech forests

Dissolved organic carbon (DOC) from Oa horizons has been proposed to be an important contributor for subsoil organic carbon stocks. We investigated the fate of DOC by directly injecting a DOC solution from ¹³C labelled litter into three soil depths at beech forest sites. Fate of injected DOC was quantified with deep drilling soil cores down to 2 m depth, 3 and 17 months after the injection. 27 ± 26% of the injected DOC was retained after 3 months and 17 ± 22% after 17 months. Retained DOC was to 70% found in the first 10 cm below the injection depth and on average higher in the topsoil than in the subsoil. After 17 months DOC in the topsoil was largely lost (− 19%) while DOC in the subsoil did not change much (− 4.4%). Data indicated a high stabilisation of injected DOC in the subsoils with no differences between the sites. Potential mineralisation as revealed by incubation experiments however, was not different between DOC injected in topsoil or subsoils underlining the importance of environmental factors in the subsoil for DOC stabilisation compared to topsoil. We conclude that stability of DOC in subsoil is primary driven by its spatial inaccessibility for microorganisms after matrix flow while site specific properties did not significantly affect stabilisation. Instead, a more fine-textured site promotes the vertical transport of DOC due to a higher abundance of preferential flow paths.

     

Temperature response of permafrost soil carbon is attenuated by mineral protection

Climate change in Arctic ecosystems fosters permafrost thaw and makes massive amounts of ancient soil organic carbon (OC) available to microbial breakdown. However, fractions of the organic matter (OM) may be protected from rapid decomposition by their association with minerals. Little is known about the effects of mineral‐organic associations (MOA) on the microbial accessibility of OM in permafrost soils and it is not clear which factors control its temperature sensitivity. In order to investigate if and how permafrost soil OC turnover is affected by mineral controls, the heavy fraction (HF) representing mostly MOA was obtained by density fractionation from 27 permafrost soil profiles of the Siberian Arctic. In parallel laboratory incubations, the unfractionated soils (bulk) and their HF were comparatively incubated for 175 days at 5 and 15°C. The HF was equivalent to 70 ± 9% of the bulk CO₂ respiration as compared to a share of 63 ± 1% of bulk OC that was stored in the HF. Significant reduction of OC mineralization was found in all treatments with increasing OC content of the HF (HF‐OC), clay‐size minerals and Fe or Al oxyhydroxides. Temperature sensitivity (Q10) decreased with increasing soil depth from 2.4 to 1.4 in the bulk soil and from 2.9 to 1.5 in the HF. A concurrent increase in the metal‐to‐HF‐OC ratios with soil depth suggests a stronger bonding of OM to minerals in the subsoil. There, the younger ¹⁴C signature in CO₂ than that of the OC indicates a preferential decomposition of the more recent OM and the existence of a MOA fraction with limited access of OM to decomposers. These results indicate strong mineral controls on the decomposability of OM after permafrost thaw and on its temperature sensitivity. Thus, we here provide evidence that OM temperature sensitivity can be attenuated by MOA in permafrost soils.     

Effects of Soil Organic Matter Properties and Microbial Community Composition on Enzyme Activities in Cryoturbated Arctic Soils

Enzyme-mediated decomposition of soil organic matter (SOM) is controlled, amongst other factors, by organic matter properties and by the microbial decomposer community present. Since microbial community composition and SOM properties are often interrelated and both change with soil depth, the drivers of enzymatic decomposition are hard to dissect. We investigated soils from three regions in the Siberian Arctic, where carbon rich topsoil material has been incorporated into the subsoil (cryoturbation). We took advantage of this subduction to test if SOM properties shape microbial community composition, and to identify controls of both on enzyme activities. We found that microbial community composition (estimated by phospholipid fatty acid analysis), was similar in cryoturbated material and in surrounding subsoil, although carbon and nitrogen contents were similar in cryoturbated material and topsoils. This suggests that the microbial community in cryoturbated material was not well adapted to SOM properties. We also measured three potential enzyme activities (cellobiohydrolase, leucine-amino-peptidase and phenoloxidase) and used structural equation models (SEMs) to identify direct and indirect drivers of the three enzyme activities. The models included microbial community composition, carbon and nitrogen contents, clay content, water content, and pH. Models for regular horizons, excluding cryoturbated material, showed that all enzyme activities were mainly controlled by carbon or nitrogen. Microbial community composition had no effect. In contrast, models for cryoturbated material showed that enzyme activities were also related to microbial community composition. The additional control of microbial community composition could have restrained enzyme activities and furthermore decomposition in general. The functional decoupling of SOM properties and microbial community composition might thus be one of the reasons for low decomposition rates and the persistence of 400 Gt carbon stored in cryoturbated material.     

Distinct microbial communities associated with buried soils in the Siberian tundra

Cryoturbation, the burial of topsoil material into deeper soil horizons by repeated freeze–thaw events, is an important storage mechanism for soil organic matter (SOM) in permafrost-affected soils. Besides abiotic conditions, microbial community structure and the accessibility of SOM to the decomposer community are hypothesized to control SOM decomposition and thus have a crucial role in SOM accumulation in buried soils. We surveyed the microbial community structure in cryoturbated soils from nine soil profiles in the northeastern Siberian tundra using high-throughput sequencing and quantification of bacterial, archaeal and fungal marker genes. We found that bacterial abundances in buried topsoils were as high as in unburied topsoils. In contrast, fungal abundances decreased with depth and were significantly lower in buried than in unburied topsoils resulting in remarkably low fungal to bacterial ratios in buried topsoils. Fungal community profiling revealed an associated decrease in presumably ectomycorrhizal (ECM) fungi. The abiotic conditions (low to subzero temperatures, anoxia) and the reduced abundance of fungi likely provide a niche for bacterial, facultative anaerobic decomposers of SOM such as members of the Actinobacteria, which were found in significantly higher relative abundances in buried than in unburied topsoils. Our study expands the knowledge on the microbial community structure in soils of Northern latitude permafrost regions, and attributes the delayed decomposition of SOM in buried soils to specific microbial taxa, and particularly to a decrease in abundance and activity of ECM fungi, and to the extent to which bacterial decomposers are able to act as their functional substitutes.     

Soil phosphorus supply controls P nutrition strategies of beech forest ecosystems in Central Europe

Phosphorus availability may shape plant–microorganism–soil interactions in forest ecosystems. Our aim was to quantify the interactions between soil P availability and P nutrition strategies of European beech (Fagus sylvatica) forests. We assumed that plants and microorganisms of P-rich forests carry over mineral-bound P into the biogeochemical P cycle (acquiring strategy). In contrast, P-poor ecosystems establish tight P cycles to sustain their P demand (recycling strategy). We tested if this conceptual model on supply-controlled P nutrition strategies was consistent with data from five European beech forest ecosystems with different parent materials (geosequence), covering a wide range of total soil P stocks (160–900 g P m^?2; <1 m depth). We analyzed numerous soil chemical and biological properties. Especially P-rich beech ecosystems accumulated P in topsoil horizons in moderately labile forms. Forest floor turnover rates decreased with decreasing total P stocks (from 1/5 to 1/40 per year) while ratios between organic carbon and organic phosphorus (C:P_org) increased from 110 to 984 (A horizons). High proportions of fine-root biomass in forest floors seemed to favor tight P recycling. Phosphorus in fine-root biomass increased relative to microbial P with decreasing P stocks. Concomitantly, phosphodiesterase activity decreased, which might explain increasing proportions of diester-P remaining in the soil organic matter. With decreasing P supply indicator values for P acquisition decreased and those for recycling increased, implying adjustment of plant–microorganism–soil feedbacks to soil P availability. Intense recycling improves the P use efficiency of beech forests.