Soil Organic Phosphorus Transformations During Pedogenesis

Abstract Long-term changes in soil phosphorus influence ecosystem development and lead to a decline in the productivity of forests in undisturbed landscapes. Much of the soil phosphorus occurs in a series of organic compounds that differ in their availability to organisms, but changes in the relative abundance of these compounds during pedogenesis remain unknown. We used alkaline extraction and solution phosphorus-31 nuclear magnetic resonance spectroscopy to assess the chemical nature of soil organic phosphorus along a 120,000-year post-glacial chronosequence at Franz Josef, New Zealand. Inositol phosphates, DNA, phospholipids, and phosphonates accumulated rapidly during the first 500 years of soil development characterized by nitrogen limitation of biological productivity, but then declined slowly to low concentrations in older soils characterized by intense phosphorus limitation. However, the relative contribution of the various compounds to the total organic phosphorus varied along the sequence in dramatic and surprising ways. The proportion of inositol hexakisphosphate, conventionally considered to be relatively recalcitrant in the environment, declined markedly in older soils, apparently due to a corresponding decline in amorphous metal oxides, which weather to crystalline forms during pedogenesis. In contrast, the proportion of DNA, considered relatively bioavailable in soil, increased continually throughout the sequence, due apparently to incorporation within organic structures that provide protection from biological attack. The changes in soil organic phosphorus coincided with marked shifts in plant and microbial communities, suggesting that differences in the forms and bioavailability of soil organic phosphorus have ecological significance. Overall, the results strengthen our understanding of phosphorus transformations during pedogenesis and provide important insight into factors regulating the composition of soil organic phosphorus.     

Vegetation Composition Determines Microbial Activities in a Boreal Forest Soil

Abstract Forest soil ecology was studied in Fennoscandinavian dry Scots pine forests grazed by reindeer to varying extents (ungrazed, lichen-dominated-sites; grazed sites; and bryophyte-dominated sites). We hypothesized that the productivity parameters of the site (i.e., tree growth and soil nutrient concentrations), the vegetation composition, and the microbial activities are directly correlated. Since the productivity of the lichen-dominated ecosystem is low, microbial activities are assumed to be naturally low. Grazing was expected to decrease both the amount of Scots pine fine roots and the soil microbial activities. Several variables on the characteristics of the soil microbial community, Scots pine fine roots, soil nutrients, and tree growth were studied in relation to vegetation composition by using non-metric multidimensional scaling (NMDS). Basal respiration (Bas), metabolic quotient of the microbial community (qCO2), and pine fine root parameters increased toward the ungrazed, nutrient-poor, lichen-dominated sites, which were grouped at one end of the first axis in the NMDS ordination. Soil nutrient and tree growth parameters and thickness of the humus layer increased toward bryophyte-dominated sites, which were grouped at the other end of the first axis in the ordination. The grazed sites fell between them. These were characterized by lower Bas and qCO2 values and longer lag, compared to ungrazed lichen- or bryophyte-dominated sites, probably due to decreased carbon input and microclimatic change (the soil without lichen carpet is exposed to direct sunlight and wind). Microbial biomass (Cmic), fungal biomass (ergosterol concentration), and the specific growth rate (μCO2) were not related to vegetation ordination. The high fine root production is the most plausible explanation for the high microbial activities at nutrient-poor, lichen-dominated sites, which produce qualitatively poor and slowly decomposing litter, as fine roots secrete considerable amounts of organic substances. At bryophyte-dominated sites, the higher soil nutrient concentrations and the higher production of easily decomposable substrates are likely to maintain the microbial activities.     

Microbial Assemblages in Soil Microbial Succession After Glacial Retreat in Svalbard (High Arctic)

Microbial community composition (cyanobacteria and eukaryotic microalgae abundance and diversity, bacterial abundance, and soil respiration) was studied in subglacial and periglacial habitats on five glaciers near Ny-Alesund, Svalbard (79 degrees N). Soil microbial communities from nonvegetated sites (subglacial, recently deglaciated, and cryoconite sediments) and sites with plant cover (deglaciated some hundreds of years ago) were analyzed. Physicochemical analyses (pH, texture, water content, organic matter, total C and N content) were also performed on the samples. In total, 57 taxa of 23 genera of cyanobacteriaand algae were identified. Algae from the class Chlorophyceae (25 species) and cyanobacteria (23 species) were richest in biodiversity. The numbers of identified species in single habitat types were 23 in subglacial, 39 inbarren, 22 in cryoconite, and 24 in vegetated soils. The highest cyanobacterial and algal biovolume and cell numbers, respectively, were present in cryoconite (13x10(4) microm3 mg-1 soil and 508 cells per mg of soil), followed by barren (5.7x10(4) and 188), vegetated (2.6x10(4) and 120), and subglacial (0.1x10(4) and 5) soils. Cyanobacteria prevailed in all soil samples. Algae (mainly green algae) were present only as accessory organisms. The density of bacteria showed a slightly different trend to that of the cyanobacterial and algal assemblages. The highest number of bacteria was present in vegetated (mean: 13,722x10(8) cells per mg of soil dry wt.), followed by cryoconite (3802x10(8)), barren (654x10(8)), and subglacial (78x10(8)) soils. Response of cyanobacteria and algae to physical parameters showed that soil texture and water content are important for biomass development. In addition, it is shown that nitrogen and water content are the main factors affecting bacterial abundance and overall soil respiration. Redundancy analysis (RDA) with forward selection was used to create a model explaining variability in cyanobacterial, algal, and bacterial abundance. Cryoconites accounted for most of the variation in cyanobacteria and algae biovolume, followed by barren soils. Oscillatoriales, desmids, and green coccoid algae preferred cryoconites, whereas Nostocales and Chroococcales occurred mostly in barren soils. From the data obtained, it is evident that of the studied habitats cryoconite sediments are the most suitable ones for the development of microbial assemblages. Although subglacial sediments do not provide as good conditions as cryoconites, they support the survival of microbial communities. Both mentioned habitats are potential sources for the microbial recolonization of freshly deglaciated soil after the glacier retreat.     

Arctic Soil Respiration: Effects of Climate and Vegetation Depend on Season

Arctic ecosystems are important in the context of global climate change because the most rapid rises in air temperature are expected at high northern latitudes during winter. The presence of extensive soil carbon reserves in the Arctic suggests that substantial feedbacks to CO₂-induced climate change could occur if warming alters carbon cycling belowground. Characterization of the controls on regional patterns of belowground CO₂ release through the annual cycle is an important step towards evaluating potential feedbacks from arctic ecosystems to climate change. In this study, we assess seasonal control over the influences by climate and vegetation-type on CO₂ efflux from belowground in the Alaskan tundra. Our results indicate that climate had strong effects on belowground CO₂ release in both seasons. By contrast, vegetation-type had little impact on CO₂ efflux from belowground in winter but was the principal control in summer. Together, these results demonstrate that seasonality is a critical factor regulating climate and vegetation-type effects on belowground CO₂ release, which should be included in regional models of net carbon balance in arctic ecosystems. Received 8 December 1998; accepted 2 April 1999.     

Aggregate Stabilization of Volcanic Ash and Soil During Microbial Degradation of Straw

Bacterial and fungal colonists of straw in soil promoted aggregate stabilization of volcanic ash and soil.     

Interactive Effects of Nitrogen and Phosphorus on Soil Microbial Communities in a Tropical Forest

Elevated nitrogen (N) deposition in humid tropical regions may exacerbate phosphorus (P) deficiency in forests on highly weathered soils. However, it is not clear how P availability affects soil microbes and soil carbon (C), or how P processes interact with N deposition in tropical forests. We examined the effects of N and P additions on soil microbes and soil C pools in a N-saturated old-growth tropical forest in southern China to test the hypotheses that (1) N and P addition will have opposing effects on soil microbial biomass and activity, (2) N and P addition will alter the composition of the microbial community, (3) the addition of N and P will have interactive effects on soil microbes and (4) addition-mediated changes in microbial communities would feed back on soil C pools. Phospholipid fatty acid (PLFA) analysis was used to quantify the soil microbial community following four treatments: Control, N addition (15 g N m⁻² yr⁻¹), P addition (15 g P m⁻² yr⁻¹), and N&P addition (15 g N m⁻² yr⁻¹ plus 15 g P m⁻² yr⁻¹). These were applied from 2007 to 2011. Whereas additions of P increased soil microbial biomass, additions of N reduced soil microbial biomass. These effects, however, were transient, disappearing over longer periods. Moreover, N additions significantly increased relative abundance of fungal PLFAs and P additions significantly increased relative abundance of arbuscular mycorrhizal (AM) fungi PLFAs. Nitrogen addition had a negative effect on light fraction C, but no effect on heavy fraction C and total soil C. In contrast, P addition significantly decreased both light fraction C and total soil C. However, there were no interactions between N addition and P addition on soil microbes. Our results suggest that these nutrients are not co-limiting, and that P rather than N is limiting in this tropical forest.     

Overexpressing AtPAP15 Enhances Phosphorus Efficiency in Soybean

Low phosphorus (P) availability is a major constraint to crop growth and production, including soybean (Glycine max), on a global scale. However, 50% to 80% of the total P in agricultural soils exists as organic phosphate, which is unavailable to plants unless hydrolyzed to release inorganic phosphate. One strategy for improving crop P nutrition is the enhanced activity of acid phosphatases (APases) to obtain or remobilize inorganic phosphate from organic P sources. In this study, we overexpressed an Arabidopsis (Arabidopsis thaliana) purple APase gene (AtPAP15) containing a carrot (Daucus carota) extracellular targeting peptide in soybean hairy roots and found that the APase activity was increased by 1.5-fold in transgenic hairy roots. We subsequently transformed soybean plants with AtPAP15 and studied three homozygous overexpression lines of AtPAP15. The three transgenic lines exhibited significantly improved P efficiency with 117.8%, 56.5%, and 57.8% increases in plant dry weight, and 90.1%, 18.2%, and 62.6% increases in plant P content, respectively, as compared with wild-type plants grown on sand culture containing phytate as the sole P source. The transgenic soybean lines also exhibited a significant level of APase and phytase activity in leaves and root exudates, respectively. Furthermore, the transgenic lines exhibited improved yields when grown on acid soils, with 35.9%, 41.0%, and 59.0% increases in pod number per plant, and 46.0%, 48.3%, and 66.7% increases in seed number per plant. Taken together, to our knowledge, our study is the first report on the improvement of P efficiency in soybean through constitutive expression of a plant APase gene. These findings could have significant implications for improving crop yield on soils low in available P, which is a serious agricultural limitation worldwide.Phosphorus (P) is a critical macronutrient for plant growth and development. Terrestrial plants generally take up soil P in its inorganic form (Pi; Marschner, 1995). However, 50% to 80% of the total P in agricultural soils exists as organic phosphate, in which, up to 60% to 80% is myoinositol hexakisphosphate (phytate; Iyamuremye et al., 1996; Turner et al., 2002; George and Richardson, 2008). Since phytate-P is not directly available to plants, low P availability becomes one of the limiting factors to plant growth.Plants have developed a number of adaptive mechanisms for better growth on low-P soils, including changes in root morphology and architecture, activation of high-affinity Pi transporters, improvement of internal phosphatase activity, and secretion of organic acids and phosphatases (Raghothama, 1999; Vance et al., 2003). Acid phosphatases (APases) are hydrolytic enzymes with acidic pH optima that catalyze the breakdown of P monoesters to release Pi from organic P compounds, and therefore may play an important role in P nutrition (Vincent et al., 1992; Li et al., 2002). APase activity, including extracellular and intracellular APase activity, is generally increased by Pi starvation in higher plants (Duff et al., 1994). Intracellular APases might play a role in internal Pi homeostasis through remobilization of Pi from older leaves and vacuole stores, whereas extracellular APases are believed to be involved in external P acquisition by mobilizing Pi from organic P compounds (Duff et al., 1994). In the last few years, secreted APases have been purified and characterized in some model plants, such as Arabidopsis (Arabidopsis thaliana; Coello, 2002) and tobacco (Nicotiana tabacum; Lung et al., 2008). Furthermore, an Arabidopsis pup3 mutation that underproduced secreted APases in root tissues accumulated 17% less P in shoots when organic P was supplied as the major P source (Tomscha et al., 2004), indicating the possible role of APases during plant growth in response to Pi starvation.Phytase is a special type of APases with the capability to hydrolyze phytate and its derivatives, which are the predominant inositol phosphates present in seeds and soils. It is generally believed that phytase activation in seeds or resynthesis in plants plays important roles in Pi remobilization through hydrolyzing the phytate into Pi during seed germination (Loewus and Murthy, 2000). Furthermore, phytase in roots and/or root exudation has been demonstrated to be important for utilizing Pi from phytate in the growth medium (Asmar, 1997; Li et al., 1997; Hayes et al., 1999; Richardson et al., 2000).AtPAP15, a purple APase with confirmed phytase activity from Arabidopsis, can hydrolyze myoinositol hexakisphosphate, yielding myoinositol and Pi (Zhang et al., 2008). Overexpression of AtPAP15 in Arabidopsis significantly decreased phytate content in leaves (Zhang et al., 2008). Sequence analysis indicates that AtPAP15 exhibits 74% similarity to the soybean (Glycine max) phytase gene, GmPhy (Hegeman and Grabau, 2001). It seems likely that the possible involvement of phytase in plant P nutrition might be conserved among different plant species. But it is still unclear whether AtPAP15 or other phytases can be used to directly help crops, including the major agronomic crop, soybean, to acquire P under low-P conditions.Soybean is one of the most important food crops, accounting for a large segment of the world market in oil crops and also serving as an important protein source for both human consumption and animal feed (Kereszt et al., 2007). Soybean is mainly cultivated in tropic, subtropic, and temperate areas, where the soils are low in P due to intensive erosion, weathering, and strong P fixation by free iron and aluminum oxides (Sample et al., 1980; Stevenson, 1986). Low P availability is especially problematic for soybean, since root nodules responsible for nitrogen fixation have a high P requirement (Robson, 1983; Vance, 2001).In this study, the Arabidopsis PAP15 gene directed by an extracellular targeting sequence from a carrot (Daucus carota) extensin gene was successfully transformed into both soybean hairy roots and whole soybean plants. Overexpression of AtPAP15 not only increased the secretion of APase from transgenic soybean hairy roots and roots of whole transgenic soybean plants, but also significantly improved APase activity in leaves, as well as P efficiency and yield in the transgenic soybean lines. To the best of our knowledge, this is the first report on the improvement of P efficiency in crop plants through constitutive expression of a plant APase gene. This study could have significant implications for improving crop production on low-P soils, which is a serious agronomic limitation worldwide.     

Microbial Life beneath a High Arctic Glacier

The debris-rich basal ice layers of a high Arctic glacier were shown to contain metabolically diverse microbes that could be cultured oligotrophically at low temperatures (0.3 to 4°C). These organisms included aerobic chemoheterotrophs and anaerobic nitrate reducers, sulfate reducers, and methanogens. Colonies purified from subglacial samples at 4°C appeared to be predominantly psychrophilic. Aerobic chemoheterotrophs were metabolically active in unfrozen basal sediments when they were cultured at 0.3°C in the dark (to simulate nearly in situ conditions), producing ¹⁴CO₂ from radiolabeled sodium acetate with minimal organic amendment (≥38 μM C). In contrast, no activity was observed when samples were cultured at subfreezing temperatures (≤−1.8°C) for 66 days. Electron microscopy of thawed basal ice samples revealed various cell morphologies, including dividing cells. This suggests that the subglacial environment beneath a polythermal glacier provides a viable habitat for life and that microbes may be widespread where the basal ice is temperate and water is present at the base of the glacier and where organic carbon from glacially overridden soils is present. Our observations raise the possibility that in situ microbial production of CO₂ and CH₄ beneath ice masses (e.g., the Northern Hemisphere ice sheets) is an important factor in carbon cycling during glacial periods. Moreover, this terrestrial environment may provide a model for viable habitats for life on Mars, since similar conditions may exist or may have existed in the basal sediments beneath the Martian north polar ice cap.     

Small Thaw Ponds: An Unaccounted Source of Methane in the Canadian High Arctic

Thawing permafrost in the Canadian Arctic tundra leads to peat erosion and slumping in narrow and shallow runnel ponds that surround more commonly studied polygonal ponds. Here we compared the methane production between runnel and polygonal ponds using stable isotope ratios, ¹⁴C signatures, and investigated potential methanogenic communities through high-throughput sequencing archaeal 16S rRNA genes. We found that runnel ponds had significantly higher methane and carbon dioxide emissions, produced from a slightly larger fraction of old carbon, compared to polygonal ponds. The methane stable isotopic signature indicated production through acetoclastic methanogenesis, but gene signatures from acetoclastic and hydrogenotrophic methanogenic Archaea were detected in both polygonal and runnel ponds. We conclude that runnel ponds represent a source of methane from potentially older C, and that they contain methanogenic communities able to use diverse sources of carbon, increasing the risk of augmented methane release under a warmer climate.     

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.     

Soil Phosphorus Fractionation and Phosphorus-Use Efficiency of a Bornean Tropical Montane Rain Forest During Soil Aging With Podozolization

We compared phosphorus (P) dynamics and plant productivity in two montane tropical rain forests (Mount Kinabalu, Borneo) that derived from similar parent materials (largely sedimentary rocks) and had similar climates but differed in terms of soil age. The younger site originated from Quaternary colluvial deposits, whereas the older site had Tertiary-age material. The older site had a distinctive spodic horizon, reduced levels of labile inorganic soil P, higher concentrations of recalcitrant organic soil P, and lower rates of net soil N mineralization. P fertilization led to soil nitrogen (N) immobilization in the P-deficient soil, indicating that soil N mineralization was limited by P at the P-deficient older site. Mean foliar nutrient concentration (on both a weight and an area basis) was similar at the two sites for all elements except P, which was lower at the older site. Aboveground net primary production (ANPP) was lower at the older site than at the younger one; this difference could be explained by the reduced availability of P and N (as down-regulated by P) at the older site. The relatively ample allocation of P and N to leaves, despite the reduced availability at the P-deficient old site, was attributable to its high resorption efficiency. High resorption resulted in lower concentrations of elements in leaf litter—that is, less decomposable low-quality litter. On the other hand, the concentration of leaf litter lignin was considerably lower at the older site; this appeared to be a de facto adaptive mechanism to avoid retarding litter decomposition.     

Plant Kin Recognition Enhances Abundance of Symbiotic Microbial Partner

Background

The stability of cooperative interactions among different species can be compromised by cheating. In the plant-mycorrhizal fungi symbiosis, a single mycorrhizal network may interact with many plants, providing the opportunity for individual plants to cheat by obtaining nutrients from the fungi without donating carbon. Here we determine whether kin selection may favour plant investment in the mycorrhizal network, reducing the incentive to cheat when relatives interact with a single network.

Methodology/Principal Findings

We show that mycorrhizal network size and root colonization were greater when Ambrosia artemisiifolia L. was grown with siblings compared to strangers. Soil fungal abundance was positively correlated with group leaf nitrogen, and increased root colonization was associated with a reduced number of pathogen-induced root lesions, indicating greater benefit to plants grown with siblings.

Conclusions/Significance

Plants can benefit their relatives through investment in mycorrhizal fungi, and kin selection in plants could promote the persistence of the mycorrhizal symbiosis.     

Phosphorus Enhances Uptake of Dissolved Organic Matter in Boreal Streams

Retention of carbon (C), either by physical mechanisms or microbial uptake, is a key driver of the transformation and storage of C and nutrients within ecosystems. Both the molecular composition and nutrient content of organic matter influence the rate at which it is retained in streams, but the relative influence of these characteristics remains unclear. We estimated the effects of nutrient content and molecular composition of dissolved organic C (DOC) on uptake in boreal streams by measuring rates of C retention, in situ, following introduction of leachates derived from alder, poplar, and spruce trees subject to long-term fertilization with nitrogen (N) or phosphorus (P). Leachate C:N varied approximately twofold, and C:P varied nearly 20-fold across species and nutrient treatments. Uptake of DOC was greatest for leachates derived from trees that had been fertilized with P, a finding consistent with P-limitation of uptake and/or preferential sorption of P-containing molecules. Optical measures indicated that leachates derived from the three tree species varied in molecular composition, but uptake of DOC did not differ across species, suggesting weak constraints on retention imposed by molecular composition relative to nutrient limitation. Observed coupling between P and C cycles highlights the potential for increased P availability to enhance DOC retention in headwater streams.