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Seasonal variations in sugar contents and microbial

community in a

Patricia M.Medeiros

a,b,*

Marcelo F.Fernandes ,Richard P.Dick

c,2

Bernd R.T.Simoneit a,b

a Environmental Sciences Graduate Program,Oregon State University,Corvallis,OR 97331,USA b

Environmental and Petroleum Geochemistry Group,College of Oceanic and Atmospheric Sciences,

Oregon State University,Corvallis,OR 97331,USA

Department of Crop and Soil Science,Oregon State University,Corvallis,OR 97331,USA Received 5November 2005;received in revised form 10March 2006;accepted 15March 2006

Available online 11May 2006

Abstract

The relationship among sugar concentrations,microbial community and physical variables (precipitation and soil temperature)was investigated in a ryegrass soil from January 2004to January 2005.Mono-and disaccharide sugars were extracted using a mixture of dichloromethane and methanol and analyzed as their TMS derivatives by GC–MS.Changes in microbial community were assessed using phospholipid and neutral lipid fatty acids (PLFA and NLFA,respectively)analysis.The results of a one-year study showed that the seasonal variability of sugar contents found in the soil samples is mainly related to biomass or nutritional status of the fungal commu-nity.The increase in sucrose and fructose exudation by plant roots in the beginning of the growing season (early spring)may be respon-sible for the highest fungal biomass amount (PLFAs)observed in this study.Fungal storage lipid abundances (NLFAs)peaked in summer,during the same period that the highest concentrations of mannitol and trehalose were detected.This is consistent with these two sugars being stress-induced fungal metabolites,produced due to the low soil moisture observed during this season.In contrast,bacterial community growth seems to be more dependent on plant substrate than on physical variables,since the strongest decrease in bacterial biomass amounts (PLFAs)was found after cutting of the ryegrass ?eld in early July.ó2006Elsevier Ltd.All rights reserved.

Keywords:Sugars;Phospholipid fatty acids;Neutral lipid fatty acids;Microbial community;Ryegrass;Seasonal variations

1.Introduction

Soil is a complex mixture of numerous inorganic and organic constituents that vary in size,shape,chemical con-stitution and reactivity,and hosts numerous organisms.The biological,chemical and physical processes involved

in soil organic matter (SOM)turnover can partly be deduced from the dynamics of soil carbohydrates (Ame-lung et al.,1999).Total sugars have been estimated to con-stitute 10%on average of SOM,occurring in living and decaying organisms,as well as in extracellular materials (Mehta et al.,1961).Soil carbohydrates have been known to in?uence soil structure,chemical processes,plant nutri-tion and microbial activity.The sources of sugars in soils are:(a)plants (the primary source);(b)animals (the minor source);and (c)microorganisms (fungi,bacteria,algae)(Mehta et al.,1961).Plant-derived sugars are a source of energy and carbon for the soil fauna and microorganisms.In turn,the microorganisms resynthesize primary hexoses and release them to the soil (Cheshire,1979;Oades,

Corresponding author.Address:104COAS Administration Building,Oregon State University,Corvallis,OR 97331,USA.Tel.:+15417372741;fax:+15417372064.

E-mail address:medeirop@https://www.wendangku.net/doc/0514147501.html, (P.M.Medeiros).1

Present address:Embrapa –Tabuleiros Costeiros,Aracaju,SE 49025-040,Brazil.2

Present address:School of Natural Resources,The Ohio State University,Columbus,OH 43210,USA.

https://www.wendangku.net/doc/0514147501.html,/locate/chemosphere

Chemosphere 65(2006)832–839

1984).Therefore,both concentration and composition of the soil’s carbohydrates can be used to assess plant-microbe relationships in SOM dynamics(Amelung et al., 1999).

Microbial biomarkers are chemical components of microorganisms,which can be interpreted(both quantita-tively and qualitatively)in terms of in situ microbial biomass,i.e.,used to characterize soil microbial communi-ties.One of the most common biomarkers are fatty acids derived from membrane lipids because they are essential components of every living cell and have structural diversity coupled with high biological speci?city(Salomonova′et al., 2003).The use of phospholipid fatty acid(PLFA)pattern as a way to acquiring a view of the microbial community in environmental samples has become increasingly popular since the work of White et al.(1979),and the methodology has now been used in many di?erent habitats such as water, sediments,bio-?lms,rhizospheres and soil(Ba?a?th,2003),as well as an index for soil alteration(Puglisi et al.,2005). More recently,neutral lipid fatty acids have been investi-gated as a measure of nutritional status of soil fungi,as neutral lipids(mainly triacylglycerols)are an important form of C and energy storage in eukaryotes(Olsson et al., 1997;Ba?a?th,2003).

The understanding of microbial biomass in regulating soil ecosystem processes(e.g.,organic matter decomposi-tion and nutrient cycling)is of particular interest for grass ?elds.Grassland ecosystems,which present a high turnover of shoot and root material and consequently a large pool of organic matter at the soil surface,support a uniquely active soil microbial community(Grayston et al.,2001).Accord-ing to Parton et al.(1987),microbial activity in grasslands was shown to increase with increasing soil temperature and soil moisture.In turn,the litter production in native grass-lands of North America was found to be linearly related to precipitation but not to temperature(Sala et al.,1988). This suggests that the contribution of carbohydrates derived from plants and microorganisms to soil organic matter depends on temperature and precipitation.Seasonal variations in sugar composition were reported for ectomy-corrhizas(Niederer et al.,1992)and soils(Hackl et al., 2000)from temperate forest stands.For grass soils, changes in carbohydrate composition were characterized for distinct climatic conditions(Amelung et al.,1999), while microbial community variability was reported over a one-year period by Grayston et al.(2001);however,the relationship between sugar contents and soil microbial composition in response to environmental variables has not been addressed before.In addition,there is a need to identify saccharides and understand their production dynamics in soils because they are potential organic tracers for the release of soil dust from the ground into the atmo-sphere(Simoneit et al.,2004).Therefore,the purpose of this study is to identify and quantify the major sugars in soil of a ryegrass?eld and characterize the relationship between the variations of the saccharide concentration and soil microbial community over an annual cycle.2.Experimental methods

2.1.Sample collection

Soil samples were taken at the end of each month from a 60ha perennial ryegrass?eld(Lolium perenne L.)located in the Willamette Valley,Oregon,USA from January2004to January2005.Four to?ve surface soils(0–3cm depth) were collected in an approximated20m diameter area and homogenized to give one composited sample.Each sample was immediately taken to the laboratory,where it was divided into two portions to carry out the sugar and fatty acid analyses.Analyses of composited samples from four di?erent parts of the?eld demonstrated that the spa-tial variability of the compound concentrations is one order of magnitude smaller than the variability between seasons over an annual cycle.The soil was classi?ed as?ne, smectitic,and mesic Typic Albaqualfs,with a pH range between 4.2and 4.6(1:2;soil:water suspension)and TOC=4.1%(dry combustion;WR12Leco Carbon Ana-lyzer,St.Joseph,MI).Soil temperatures and precipitation levels were recorded at an automated weather station (OCS,2005)located approximately5km from the sam-pling site.

2.2.Sugar analysis

Soil samples were dried at room temperature,grounded and sieved with600l m pore-size mesh in order to remove vegetation and plant root fragments.Approximately10g of soil was sonicated twice for15min in a30ml mixture of dichloromethane:methanol(2:1,v/v).The extract ali-quots were combined,?ltered and concentrated by rotary evaporator to about1.5ml,then further to about500l l using a stream of high purity nitrogen.Aliquots of the total extracts were converted to their trimethylsilyl derivatives using N,O-bis-(trimethylsilyl)tri?uoroacetamide(BSTFA) containing1%trimethylchlorosilane(TMCS)and pyridine (Pierce)for3h at70°C.An aliquot of1l l of each silylated total extract of the soil samples was analyzed within24h using a HP(now Agilent)6890gas chromatograph inter-faced with a HP5973mass selective detector(GC–MS).

A DB5-MS capillary column(30m·0.25mm i.d.and?lm thickness of0.25l m,Agilent)was used with helium as the carrier gas at a constant?ow rate of1.3ml minà1.The injector and MS source temperatures were maintained at 280°C and230°C,respectively.The column temperature program consisted of injection at65°C and hold for 2min,temperature increase of6°C minà1to300°C,fol-lowed by an isothermal hold at300°C for15min.The MSD was operated in the electron impact mode with an ionization energy of70eV.The scan range was set from 50to650Da at1.27scan sà1.The samples were analyzed in the splitless mode(splitless time:30s).

Data were acquired and processed with the HP(Agilent) Chemstation software.Individual sugars were identi?ed by comparison of mass spectra with literature and library

P.M.Medeiros et al./Chemosphere65(2006)832–839833

data,comparison of mass spectra and GC retention times with those authentic standards and/or interpretation of mass spectrometric fragmentation https://www.wendangku.net/doc/0514147501.html,pounds were quanti?ed using total ion current(TIC)peak area and converted to compound mass using calibration curves of external standards(glucose for monosaccharides,sorbi-tol for reduced sugars and sucrose for disaccharides).Pro-cedural blanks were run in sequence to soil samples, presenting no signi?cant background interferences.Recov-eries of sugar standards were already published elsewhere (Simoneit et al.,2004)and varied from92%to97%.

2.3.Fatty acid analysis

The second portion of each soil sample was passed through a2mm sieve,and the soil lipids were extracted according to Bligh and Dyer(1959).Brie?y,10ml of a sin-gle phase chloroform–methanol-phosphate bu?er solution (1:2:0.8,v/v/v;pH4)was added to3g of moist soil.After centrifugation(repeated twice),the supernatants were com-bined and?ltered.The extract was split into two phases by adding10ml of NaCl(2M)to the chloroform–methanol-phosphate bu?er solution(Folch et al.,1957).The ex-tracted lipids,present in the chloroform phase,were then fractionated into neutral,intermediate,and polar lipids by elution with10ml of chloroform,10ml of acetone,and 10ml of methanol,respectively,using silicic acid bonded phase columns(SPE-SI;Supelco)previously conditioned with3ml of chloroform(Zelles and Bai,1993).The neutral lipids(storage lipids)and polar lipids(containing phospho-lipids)were immediately dried under nitrogen.The samples were then subjected to alkaline methanolysis using methan-olic KOH0.2M,which transesteri?ed the fatty acids derived from neutral and phospholipids into free fatty acid methyl esters(FAMEs)(Butler et al.,2003).The methyl-ated compounds were analyzed by gas chromatography with a HP5890Series II equipped with a HP Ultra-2capil-lary column(25m·0.2mm i.d.and?lm thickness of 0.33l m)and?ame ionization detector(GC-FID).Helium was used as the carrier gas at a?ow rate of0.8ml minà1. The injector and detector temperatures were250°C and 280°C,respectively.The temperature program ramped from120to290°C at5°C minà1and5min at290°C between samples to clean the column.Soil extracts(1l l) were injected in the splitless mode(splitless time:45s). Peaks were identi?ed using a mixture of37FAMEs (FAME37;Supelco)and24bacterial FAMEs(P-BAME 24;Supelco).Methyl tridecanoate(13:0;Supelco)was used as an internal standard to convert chromatographic areas into FAME concentrations.Procedural blank analyses were carried out and did not present signi?cant interfer-ences.Fatty acid recoveries were already published(Zelles and Bai,1993)and varied from98%to99.6%.

The nomenclature of the fatty acids follows that used by Frostega?rd et al.(1993).The polyenoic unsaturated PLFA 18:2x6was used as an indicator of fungal biomass(Fed-erle,1986;Frostega?rd and Ba?a?th,1996),whereas NLFA 18:2x6was used as a fungal storage indicator(Ba?a?th, 2003).It was assumed that the primary source of this eukaryotic PLFA and NLFA was soil fungi(Zogg et al., 1997;Ba?a?th,2003).Gram-positive bacteria were repre-sented by the branched PLFAs i15:0,a15:0,i16:0,i17:0, a17:0,whereas the PLFAs18:1x7,cy19:0,cy17:0were cho-sen to represent Gram-negative bacteria(Federle,1986; O’Leary and Wilkinson,1988;Wilkinson,1988).The satu-rated PLFAs10Me16:0,10Me17:0,10Me18:0were taken to represent actinomycete biomass(O’Leary and Wilkin-son,1988;Kroppenstedt,1992).

2.4.Correlation analysis

In order to examine the interrelation between sugar con-tents and soil microbial composition over an annual cycle in the soil samples,correlation coe?cients among individ-ual sugar concentrations(mono-and disaccharides),soil microbial abundances(fungal and bacterial fatty acids) and climatic variables(soil temperature and precipitation) were calculated.

3.Results

3.1.Environmental variables

The seasonal variability of the soil temperatures and total precipitation recorded close to the sampling site dur-ing January2004–January2005is shown in Fig.1.The low-est soil temperature(5.1°C)and highest precipitation (211mm)were observed in January2004when a short snow event occurred in the beginning of the month.The summer season was marked by the highest temperatures and lowest precipitation recorded during the whole period(e.g.,July with averaged soil temperatures and precipitation of about 26.2°C and<1mm,respectively).In addition,comparisons to averaged values recorded since1996showed that the period from November2004to January2005was charac-terized by lower precipitation levels(summed total precipi-tation for the three months$234mm,summed departure à282mm)and higher air temperatures(mean temperature $6°C,mean departure+1°C)(OCS,2005).

In early July,the ryegrass canopy was harvested and its aboveground biomass removed from the sampling site.In the subsequent months,a progressive regrowth of the grass was observed.

3.2.Sugar analysis

The individual concentrations of the monosaccharides glucose,fructose and mannitol(reduced sugar),and the disaccharides sucrose and trehalose(also known as mycose)present in soil samples taken from the Oregon rye-grass?eld are shown in Fig.2.Total sugar concentrations varied from approximately3765to23710ng gà1with maxi-mum concentrations found in samples collected in the sum-mer season,i.e.,from June to September.The disaccharide

834P.M.Medeiros et al./Chemosphere65(2006)832–839

trehalose was by far the most abundant sugar found in the soil samples during the study period,ranging from about 3495to 19834ng g à1,followed by the disaccharide sucrose ($144–2853ng g à1).Trehalose is a recognized fungal car-bohydrate (Martin et al.,1988;Niederer et al.,1989),while sucrose is the predominant sugar in the phloem of plants (Bieleski,1995).Glucose is the most common sugar in nat-ure (Pigman and Horton,1970),and here it was the most abundant monosaccharide found,varying from approxi-mately 100to 2242ng g à1.Sugar concentrations presented a strong seasonal variability.As the growing season pro-gressed,glucose increased to a maximum in July.After that,a strong decrease was observed to a minimum in October,when the concentrations progressively increased.The monosaccharide fructose and the disaccharide sucrose (a dimer of glucose and fructose)were prevalent in early spring,when the climatic conditions were milder.In con-

trast,the reduced sugar mannitol and the disaccharide tre-halose had higher concentrations in late spring and summer,the period of highest soil temperatures and lowest precipitation (Fig.1).3.3.FAME analysis

Fatty acid methyl esters (FAMEs)were used to study changes in both the phospholipid and neutral lipid frac-tions.Both phospholipid and neutral lipid amounts were calculated from the sum of individual fatty acids (when applicable)and are shown in Fig.3as their relative abun-dances,i.e.,(value –mean)/standard deviation.Fig.3a shows the seasonal variations of fungal fatty acid amounts in the soil samples collected from February 2004to Janu-ary 2005.Phospholipid fatty acids (PLFAs),used to indi-cate fungal biomass (Federle,1986;Frostega

?rd

and

P.M.Medeiros et al./Chemosphere 65(2006)832–839

835

Ba?a?th,1996;Tunlid and White,1992),strongly increased from the beginning of the year to a maximum in April (early spring),when a progressive decrease was observed until October.The neutral lipid fatty acid amounts (NLFAs),indicative of fungal storage lipids(Olsson and Wilhelmsson,2000;Ba?a?th,2003),increased until April sim-ilar to the PLFA amounts.However,in contrast to the fun-gal biomass,the fungal storage abundances increase to a maximum in the summer season(June and July),when highest temperatures and lowest precipitation levels were recorded(Fig.1).After that time,the NLFA amounts strongly decrease until September,when a slight increase was observed by the end of the year(early winter),identical to the fungal biomass(PLFA amounts).

Variations in the bacterial fatty acid relative abundances from February2004to January2005are shown in Fig.3b. Seasonal variations of bacterial PLFA amounts were very similar for the categories of bacteria studied here.As tem-perature increases,Gram-positive,Gram-negative and acti-nomycete fatty acid amounts also increase to a maximum in late spring/early summer.In July,bacterial lipid abun-dances strongly decreased to levels that were maintained until October,when an increase was observed by the end of the study period.Neutral lipid fatty acids(NLFAs)were not determined for bacteria since their levels as storage compounds are generally low in these microorgan-isms(Neidhardt et al.,1990;Ba?a?th,2003;Malosso et al., 2004).

3.4.Correlation analysis

Correlation coe?cients among sugar contents,FAME microbial signatures and physical variables are shown in Table1.The reduced sugar mannitol is highly correlated to the disaccharide trehalose(r=0.86),and correlates pos-itively with temperature and negatively with precipitation.

A similar trend was found for fungal neutral lipid amounts (NLFAs),which correlated with mannitol and trehalose (r=0.69and0.56,respectively)and negatively with precip-itation(r=à0.56).The monosaccharide glucose is well correlated with most sugars,physical variables,fungal PLFA and NLFA,and Gram-negative bacteria,thus not indicating an association speci?city character.In contrast, the disaccharide sucrose is well correlated with fructose (r=0.80),which is correlated with the fungal biomass variations(PLFA abundances).No correlation was found among plant sugar contents(sucrose and fructose),temper-ature,precipitation and bacterial fatty acid seasonal variations.In fact,the three categories of bacteria studied (Gram-positive,Gram-negative and actinomycetes)did not have signi?cant correlations with either climatic vari-ables or sugar concentrations(except glucose).

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4.Discussion

The results presented here demonstrated that seasonal variations in sugar concentrations in a ryegrass soil are clo-sely related to the fungal fatty acid signatures.The increase in fructose,sucrose and glucose concentrations in the soil samples from the beginning of the year until April may be related to the breaking of the winter-induced dormancy. As the growing season approaches,the polysaccharides fructan and starch are subjected to hydrolysis,releasing their monomers(Wilson et al.,2001).Fructans are poly-mers of fructose and,together with starch(a glucose poly-mer)and fructose,are the major reserve carbohydrates in the roots of higher plants(Meier and Reid,1982).Increases of fructose,glucose and sucrose within plants may result in exudation of those sugars by plant roots,increasing their concentrations in the soil samples.Wilson et al.(2001) observed increases of fructose and glucose in dandelion roots in early spring due to polysaccharide hydrolysis. After April,fructose and sucrose amounts strongly decreased,probably due to the translocation of sugars to other parts of the plants for supporting growth in spring (van Doorn,2004).A similar trend was observed for fungal PLFA amounts(Fig.3a).Fungal biomass reached its max-imum in April,probably due to higher availability of those sugars in the soil(Grayston et al.,2001),which may also result in an increase of neutral lipid amounts(NLFAs) by the fungal community.

By the end of spring and during summer,a progressive decrease of the fungal PLFA amounts was observed (Fig.3a).During this period,the fungal biomass may undergo drought stress due to the lowest precipitation levels observed throughout the sampling period(Fig.1).In con-trast to the biomass of fungi,the fungal storage lipid amounts(NLFAs)reached their maximum in June and July (Fig.3a),similar to the concentrations of the reduced sugar mannitol and the disaccharide trehalose(Fig.2).The conversion of fructose,glucose and sucrose into the fungus speci?c metabolites trehalose and mannitol has been reported for excised ectomycorrhizal symbiosis(Lewis and Harley,1965;Martin et al.,1985,1988).Both sugars are known as reserve carbohydrates in microorganisms,primar-ily fungi(Martin et al.,1988;Sillje′et al.,1999).Mannitol is also an intracellular osmoregulatory solute,accumulating in stressed cells to adjust their osmotic potential to salt stress and water de?ciency(Shen et al.,1999;Ramirez et al., 2004),while trehalose is a stress protectant to dehydration and freezing,as well as osmostress and carbon starvation (Niederer et al.,1992;Sillje′et al.,1999).Additionally, perennial ryegrasses store carbohydrates as mainly fructan, which is hydrolyzed to sucrose,fructose and glucose upon drought and defoliation(Karsten and MacAdam,2001). In fact,an increase of those sugars was also observed during the dry months(Fig.2).These results support the conten-tion that mannitol and trehalose are fungal typical metabo-lites,produced here to overcome the low precipitation levels.

The lower concentrations of the plant sugars detected by the end of summer in the soil samples are probably due to utilization of those sugars for plant regrowth,which took place during autumn,after cutting the grass.Defoliation (cutting)is a strong perturbation to plant C?ow,dramat-ically reducing photosynthetic capacity,and resulting in preferential carbon allocation above-ground at the expense of below-ground allocation(Morvan-Bertrand et al.,1999). The lowest total sugar concentrations were observed dur-ing this period(October,Fig.2),which was followed by the decrease of fatty acid amounts derived from fungal biomass(PLFAs)and storage lipids(NLFAs)(Fig.3a). Lower plant sugar abundances may be responsible for the decrease of fungi biomass growth during autumn,or possibly increased grazing of microorganisms by protozoa and nematodes,since those populations were already reported to peak in autumn in a North American tallgrass (Todd et al.,1992).

The last months of the one-year soil collection were marked by a slight increase in sugar concentrations to a

Table1

Correlation coe?cients among sugar contents,soil microbial communities and physical variables in a Ryegrass soil

Variables Glu Fru Suc Man Tre PLFA fungi NLFA fungi PLFA G+PLFA GàPLFA Actin Soil temp Glu

Fru0.59*

Suc0.230.80*

Man0.82*0.11à0.13

Tre0.60*à0.09à0.150.86*

PLFA fungi0.67*0.66*0.330.370.24

NLFA fungi0.81*0.450.080.69*0.56*0.76*

PLFA G+0.34à0.10à0.310.440.410.56*0.53

PLFA Gà0.56*0.10à0.170.510.490.71*0.73*0.93*

PLFA Actin0.05à0.20à0.420.100.110.490.300.90*0.76*

Soil temp0.63*0.180.070.77*0.78*0.260.450.130.31à0.12

Precipà0.64*à0.35à0.17à0.54*à0.43à0.35à0.56*à0.31à0.43à0.08à0.70* Glu:glucose;Fru:fructose;Suc:sucrose;Man:mannitol;Tre:trehalose;PLFA:phospholipid fatty acids;NLFA:neutral lipid fatty acids;G+:gram-positive bacteria;Gà:gram-negative bacteria;Actin:actinomycetes;Soil temp:soil temperature;Precip:precipitation.

*P<0.05.

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level similar to that found in January2004(Fig.2).This suggests that climatic variables by the end of the year were not extreme enough to result in extensive changes in the fungal biomass or nutritional status(PLFA and NLFA sig-natures,respectively)and sugar contents.

In contrast to the fungal biomass,seasonal variations in the bacterial community PLFA appear not be tied to the changes in the sugar contents in the ryegrass soil samples. As the temperature increased and precipitation decreased, bacterial fatty acid amounts increased to a maximum in late spring/early summer(Fig.3b).The strong decrease in the Gram-positive,Gram-negative and actinomycete bacteria growth detected in July is probably due to the grass being cut early that month.The soil microbial com-munity often responds to cutting independently of changes in the root biomass,suggesting that they are a?ected by changes in root exudation(Guitian and Bardgett,2000). Yang and Crowley(2000)have already reported the partic-ular importance of plant substrate(plant root exudates)for the bacterial community’s composition.In addition,as the grass regrowth progressed by the end of the sampling per-iod(reaching$30cm height),bacterial fatty acid amounts also showed a signi?cant increase(Fig.3b).

Similarly to fungi,bacteria accumulate compatible sol-utes in order to overcome stress conditions or as storage compounds(Ba?a?th,2003;Beales,2004).However,the compatible osmoregulatory solutes produced internally by bacteria include not only sugars,but also amino acids from protein degradation and cations such as K+.Exam-ples are betaine,choline,proline,ectoine,glycerol,glucitol, mannitol and trehalose(Galinski,1995).Indeed,no corre-lation was observed between the production of the stress-induced metabolites found here(trehalose and mannitol) and bacterial community changes.Also,bacteria do not store compounds as lipids but,for example,as poly-hydroxybutyric acid(Neidhardt et al.,1990).

In conclusion,the results of a one-year study in a rye-grass?eld showed that the seasonal variability of sugar contents found in the soil samples is primarily related to the changes in fungal biomass or nutritional status(PLFA and NLFA fungal signatures,respectively).In contrast, bacterial community growth seems to be more dependent on plant substrate than on climatic variables,since the strongest decrease in bacterial biomass PLFA amounts was found after cutting of the ryegrass?eld.The results also con?rm the sugars mannitol and trehalose as stress-induced fungal metabolites,triggered here by the low soil moisture observed during the summer season. Acknowledgements

PMM and MFF gratefully acknowledge the Brazilian government(CNPq–Conselho Nacional de Desenvolvi-mento Cient?′?co e Tecnolo′gico)for?nancial support (PMM Grant200330/01-2,MFF Grant200867/92-0). PMM also thanks Renato Castelao for valuable assistance during sample collection.We acknowledge the two anony-mous reviewers and the editor,who provided constructive comments which improved this paper.

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英文歌曲歌词带翻译(一)

the sound of silence 静之声- 保罗。西蒙 hello darkness my old friend. 你好，黑夜，我的老朋友 i've come to talk with you again. 我又来和你聊天了 because a vision softly creeping 因为当我熟睡的时候，一幅美景便进入了我的梦乡。 left its seeds while i was sleeping. （因为梦幻缓缓涌现，在我熟睡时留下它的种子。） and the vision that was planted in my brain 在我脑袋里的那幅美景仍然保持着寂寞之声！still remains with the sound of silence （在我脑海中生根，在寂静之声中留存。） in restless dreams i walk alone 在不安的梦中我一个人独行（在无休止的梦境中，narrow streets of cobble stone 我独自走在狭窄的石道上。） beneath the halloof a street lamp, 在街灯的光晕下，寒冷和湿气让我竖起衣领。 i turned my collar to the cold and damp when my eyes were stabbled by the flash 当霓虹灯光刺痛我双眼， of a neon light that split the night 划破黑夜， and touched the sound of silence 触动了沉默之声。 and in the naked night i saw ten thousand people may be more 在刺眼的灯光下，我看到上万人群。

最经典超好听的英文歌词--带翻译

。 1欢迎下载 My love---西域男孩 An empty street, an empty house, 空空的街道,空空的房, a hole inside my heart, 心里也是个空空的洞, I'm all alone, the rooms are getting smaller, 我孤独的一个人,房间也变得越来越小, I wonder how, I wonder why, 我不知道怎么回事,也不知道为什么, I wonder where they are, 我不知道它们哪去了, the days we had, 我们有过的好时光, the songs we sang together, oh yeah. 我们一起唱过的歌,oh,yeah. and oh my love, 还有你－－我的最爱, I'm holding on forever, 我一直在坚持, reaching for a love that seems so far. 想得到那份似乎遥不可及的爱. all:(合唱) So I say a little prayer, 所以我低声祈祷, hope my dreams will take me there, 希望我的梦会带我到那儿, where the skies are blue, 那儿天空湛蓝, to see you once again ,my love, 再次见到你,我的爱, over seas from coast to coast, 漂洋过海,从一个海岸到到另一个海岸 find the place I love the most, 找到我最爱的地方, where the fields are green, 那儿田野葱郁, i see you once again, my love. 我再一次见到你,我的爱. bryan:(Bryan 唱) I try to read, I go to work 我设法去读书,去工作, i'm laughing with my friends, 我和朋友们一起说说笑笑, but I can't stop to keep myself from thinking, oh no, 可我没法不想你,oh,no, I wonder how, i wonder why, 我不知道怎么回事,我不知道为什么, I wonder where they are, 我不知道它们哪去了, the days we had, 我们有过的好时光, the songs we sang together, oh yeah. 我们一起唱过的歌,oh yeah. and oh my love, 和你－－我的最爱, I'm holding on forever, 我一直在坚持, reaching for a love that seems so far. 想要得到那份似乎遥不可及的爱. all:(合唱) so I say a little prayer, 所以我低声音祈祷, hope my dreams will take me there, 希望我的梦会带我去那儿, where the skies are blue, 那儿天空湛蓝, to see you once again my love, 再一次见到你,我的爱, over seas from coast to coast, 穿洋过海,从一个海岸到另一个海岸 find the place i love the most, 找到我最爱的地方, where the fields are green, 那儿田野葱郁, see you once again 再一次见到你. mark:(马克唱) to hold you in my arms, 把你拥在怀里, to promise you my love, 向你承诺我的爱, to tell you from afar,

seasonsinthesun_中文歌词翻译_中英对照

Seasons?in?the?Sun_中文歌词翻译_中英对照 goodbye to you my trusted friend.再见了,我忠实的朋友. we're known each other we're 9 or 10.我们从孩提时就已相识相知. together we've climb hills trees.我们一起爬山上树. learned of love abc.一起学习. skinned our hearts skinned our knees.我们心意相通,情如手足. goodbye my friend it's hard to die.再见了，朋友们,我本不愿离去. when all the birds are singing in the sky.当所有的鸟儿在天空歌唱. now the spring is in the air.空气中弥漫着春天的气息. pretty girls are everywhere.到处是漂亮女孩. think of me and i'll be there.想我,我便与你同在. we had joy,we had fun.我们曾如此快乐. we had seasons in the sun.也曾充满阳光. but the hills that we climbed were just seasons out of time.那些日子已然逝去. goodbye papa please pray for me.再见了爸爸,请为我祈祷. i was the black sheep of the family.我是家里的害群之马. u tried 2 teach me right from wrong.你费尽心思教我明辨是非. too much wine too much song.我却沉醉于歌酒狂欢. wonder how i got along.真不知那些日子是如何度过. goodbye papa is hard 2 die.再见了爸爸,我本不愿离去. when all the birds are singing in the sky.当所有的鸟儿在天空歌唱. now the spring in the air.空气中弥漫着春天的气息. little children everywhere.孩子们到处嬉戏. when u see them i'll be there.当你看见他们,我便会与你同在. we had joy,we had fun.我们曾如此快乐. we had seasons in the sun.也曾有阳光季节. but the wild the song.但昔日的歌酒狂欢. like the season has all gone.犹如季节更迭已消逝. we had joy,we had fun.我们曾如此快乐. we had seasons in the sun.也曾有阳光季节. but the wild the song.但昔日的歌酒狂欢. like the season has all gone.犹如季节更迭已消逝. goodbye michelle my little one.再见了蜜雪儿,我的贝比. u gave me love help me find the sun.你给我爱,给我希望. and every time that i was down.当我意志消沉时.

Sugar 中文歌词

Sugar 中文歌词歌曲背景 Adam Levine表示"Sugar"是专辑《V》里自己最喜欢的，“我们乐队总喜欢创作一些吵闹的、喧嚣的歌曲，这首歌基本算是乐队最纯净和美好的歌了，我们希望这首歌能传递希望和甜蜜。” 《美国之声》第七季Adam Levine的学员Chris Jamison也唱了这首歌。2014年底，在这首歌正式打榜之前就已经备受关注，不仅因为这首歌作为尼桑汽车广告歌曲出现，而且在《美国之声》第七季里，亚当所带的学员克里斯·贾米森（Chris Jamison）在5进3比赛中演唱了这首歌。这次演唱帮助克里斯获得了高人气的投票首先晋级决赛，也让"Sugar"广泛传唱开来。 “当他找到我并说想唱这首歌时，我很震惊也很高兴，”亚当在谈及克里斯难掩喜悦，“这首歌很适合他，而且也是我们乐队自己的歌。” 中英文歌词： I'm hurting baby, I'm broken down 我很受伤，宝贝，我一蹶不振 I need your loving, loving 此时我需要你的爱，你的爱

I need it now 此刻我就迫不及待 When I'm without you 每当没有你的时候 I’m something weak 我就变得脆弱无力 You got me begging, begging 是你让我学会哀求 I'm on my knees 我不惜屈膝跪地 I don’t wanna be needing your love 我不想像现在一样哀求着你的爱 I just wanna be deep in your love 我只想深陷你的爱海 And it's killing me when you're away 当你离开我的时候，我的心也跟着死去 Ooh baby, cause a bullet don't care where you are 哦，宝贝，就像一颗不计较目的地的子弹 I just wanna be there where you are 我只想在有你的地方 And I gotta get one little taste

最经典超好听的英文歌词--带翻译

My love---西域男孩 An empty street, an empty house, 空空的街道,空空的房, a hole inside my heart, 心里也是个空空的洞, I'm all alone, the rooms are getting smaller, 我孤独的一个人,房间也变得越来越小, I wonder how, I wonder why, 我不知道怎么回事,也不知道为什么, I wonder where they are, 我不知道它们哪去了, the days we had, 我们有过的好时光, the songs we sang together, oh yeah. 我们一起唱过的歌,oh,yeah. and oh my love, 还有你－－我的最爱, I'm holding on forever, 我一直在坚持, reaching for a love that seems so far. 想得到那份似乎遥不可及的爱. all:(合唱) So I say a little prayer, 所以我低声祈祷, hope my dreams will take me there, 希望我的梦会带我到那儿, where the skies are blue, 那儿天空湛蓝, to see you once again ,my love, 再次见到你,我的爱,

over seas from coast to coast, 漂洋过海,从一个海岸到到另一个海岸 find the place I love the most, 找到我最爱的地方, where the fields are green, 那儿田野葱郁, i see you once again, my love. 我再一次见到你,我的爱. bryan:(Bryan唱) I try to read, I go to work 我设法去读书,去工作, i'm laughing with my friends, 我和朋友们一起说说笑笑, but I can't stop to keep myself from thinking, oh no, 可我没法不想你,oh,no, I wonder how, i wonder why, 我不知道怎么回事,我不知道为什么, I wonder where they are, 我不知道它们哪去了, the days we had, 我们有过的好时光, the songs we sang together, oh yeah. 我们一起唱过的歌,oh yeah. and oh my love, 和你－－我的最爱, I'm holding on forever, 我一直在坚持, reaching for a love that seems so far. 想要得到那份似乎遥不可及的爱.

昨日重现英文歌词含中文翻译

昨日重现(Yesterday once more English lyric) When I was young I'd listen to the radio 当我年少的时候，我总爱守在收音机旁 Waiting for my favorite songs 等待着我最心爱的歌曲从收音机里轻轻流淌。 When they played I'd sing along,It make me smile. 每当歌声响起，我都会独自哼唱，这时的我，心神荡漾。 Those were such happy times and not so long ago 那些真是快乐的时光，仿佛就发生在不远的身旁， How I wondered where they'd gone. 我现在多想知道美好的时光都已去向何方。 But they're back again just like a long lost friend 然而此时，他们都又回来了，就象我的一个老友一样。 All the songs I love so well.Every shalala every wo'wo 我是多么喜欢这些歌曲啊！每一个字,每一句歌词, still shines. Every shing-a-ling-a-ling that they're starting to singso fine . 仍在我心里闪耀;每一个音符，每一段旋律，仍令我心中掀起波浪。 When they get to the part 每当听到他们离别的时候； where he's breaking her heart 他伤了她的心的时候， It can really make me cry 我仍会为之哀伤。 just like before. 就象过去一样. It's yesterday once more. 一切仿佛旧日重现， (Shoobie do lang lang) 无比惆怅。 Looking back on how it was in years gone by 回过头来看看走过的岁月, And the good times that I had 和曾经美好的时光, makes today seem rather sad, 如今的生活是如此令人心伤， So much has changed. 多少东西都已改变，无法阻挡! It was songs of love that I would sing to them 只有那些关于爱的歌曲让我依就吟唱 And I'd memorize each word. 每句歌词都深深地印在我的心坎上。 Those old melodies still sound so good to me 这些远去的旋律一直默默地伴随着我， As they melt the years away 即便是岁月蹉跎，颜容消磨。

sugar歌词

I'm hurting baby, I'm broken down I need your loving, loving I need it now When I'm without you I'm something weak You got me begging, begging I'm on my knee I don't wanna be needing your love I just wanna be deep in your love And it's killing me when you're away Ooh baby,cause a bullet don't care where you are I just wanna be there where you are And I gotta get one little taste Sugar Yes please Won't you come and put it down on me Oh right here, cause I need Little love and little sympathy Yeah you show me good loving Make it alright Need a little a sweetness in my life Sugar Yes please Won't you come and put it down on me My broken pieces You put them up Don't leave me hanging, hanging Come get me some

20首流行经典英文歌词翻译

BRESSANONE（狼）布列瑟农 here i stand in bressanone 我站在布列瑟侬 with the stars up in the sky 密布着星光的苍穹下 are they shining over brenner 依稀的光照亮着布莱勒 and upon the other side 从天的那一边 you would be a sweet surrender 你送出甜蜜的笑（驻足凝望） i must go the other way 谁将被迫离去 and my train will carry me onward 离别的列车将带他远去 though my heart would surely stay 只有跳跃的心不愿离去 wo my heart would surely stay 呜跳跃的心不愿离去 now the clouds are flying by me 我多想飞起 and the moon is on the rise （融入）升起的月亮 i have left stars behind me 让群星环绕着我 they were disamondsin your skies 它们将魂绕在你的星空里 you would be a sweet surrender 你将送出甜蜜的笑（驻足凝望） i must go the other way 谁将被迫离去 and my train will carry me onward 离别的列车将带他远去 though my heart would surely stay 只有跳跃的心不愿离去 wo my heart would surely stay 呜只有跳跃的心不愿离去 cry on my shoulder 演唱:deutschl. Sucht den superstar if the hero never comes to you 如果你的真命天子总是与你擦肩而过 if you need someone you?re feeling blue

英文歌词翻译技巧

英语资源/备考辅导英文歌词翻译技巧The Rose Some say love, it is a river that drowns the tender reed. Some say love, it is a razor that leaves your soul to bleed. Some say love, it is a hunger, an endless aching need. I say love, it is a flower, and you its only seed. It's the heart afraid of breaking that never learns to dance. It's the dream afraid of waking

that never takes the chance. It's the one who won't be taken, who cannot seem to give, And the soul afraid of dying that never learns to live. When the night has been too lonely And the road has been to long And you think that love is only For the lucky and the strong Just remember in the winter Far beneath the bitter snows Lies the seed that with the sun's love In the spring becomes the rose. 学生的优秀译文（从几百份译文中，挑选出。）

english song

1、《try try》开头就能吸引住你，男生调皮地唱，尝试尝试！嗯！在失败后，尤其要不灰心！努力尝试！ 2、《i believe i can fly》这首歌大家应该很熟悉！我相信我能飞！超级励志！大推！嘿嘿~。。。。。 3、《just stand up》忘了它中文名子叫什么了，反正是很励志，给人一种拨云见天的感觉！建议看看词！很好。。。。 4、《hero》英雄。。。自始至终喜欢马里亚凯莉的高亢唱腔。。。。总是让人。。。很喜欢。每个人都是自己的英雄！不是么？ 5、《life is cool》生活很酷！呵呵~原来很喜欢糖果盒子的曲子~很甜~但有种很强烈的独立感~生活真的很酷呢~嘿嘿~ 6、《i could be the one》我是第一。。。。。很可爱的唱法~小女生~但没有女生的柔弱~一种女生能以柔克刚的坚韧~不是么~嘿嘿。。。。。 7、《feel good》一首最经典的广告歌曲~感觉很好！也算是一种自我安慰吧！最近总是哼这首歌。。。。 8、《this is me》女生的歌~这就是我。。。呵呵。。。很有爆发力！这首歌很能给我动力！希望它也能给你动力！ 9、《Bad day》或许你觉得今天是糟糕的一天？听听丹尼尔的故事吧，笑一笑，寻找遗失的美好！ 10、《breakaway》凯利克拉克森的歌，歌词很美，而且很有意义！ 11、《I have a dream》西城男孩的歌，一贯风格，深沉和缓但充满张力。其实就是说，保护你的梦想，梦想终将实现！ 12、《It's my life 》非常经典的歌了！bon jovi所唱，不必听歌词单是曲调就很振奋人心！这就是我们的人生！

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5、百度词典网址：https://www.wendangku.net/doc/0514147501.html,/ 6、海词在线翻译网址：https://www.wendangku.net/doc/0514147501.html,/ 7、金桥翻译网址：https://www.wendangku.net/doc/0514147501.html,/ 8、谷词在线词典网址：https://www.wendangku.net/doc/0514147501.html,/ 9、木头鱼在线翻译网址：https://www.wendangku.net/doc/0514147501.html,/translation/ 10、nciku在线词典网址：https://www.wendangku.net/doc/0514147501.html,/ 一、翻译质量比拼单词翻译测试项1：日常用语翻译单词：boil 参考释义：煮沸测试结果： 1、Google翻译：沸腾、煮沸等 2、Windows Live在线翻译：煮沸

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我再一次见到你,我的爱.

you you you you 让我留在你身旁

me 上帝是一个女孩 - -~~ Free Loop I'm a little used to calling outside your name

有点习惯大声叫喊你的名字 I wont see you tonight so I can keep from going insane 今晚不会见你,因此我也不会再次疯狂 But I don't know enough, I get some kinda lazy day 但,我始终不解,日子变得有些懒散了 Hey yeah 嘿耶 I've been fabulous through to fight my town a name 我曾神话般地为我的小镇添光加彩 I'll be stooped tomorrow if I don't leave as them both the same 如果我不像他们那样离开,我明天也会遭到唾弃 But i dont know enough, I get some kinda lazy day 但,我始终不解,日子变得有些懒散了 Hey yeah 嘿耶 Cause it's hard for me to lose 因为我很少失败 In my life I've found only time will tell 我发觉在我的生活中只有时间才能证明一切 And I will figure out that we can baby 我坚信我们行的,宝贝 We can do a one night stand, yeah 我们可以享受一夜露水之欢 And it's hard for me to lose in my life 我很少失败 I've found outside your skin right near the fire 我从你的热情的外表上看到我们能行 That we can baby 我们行的,宝贝 We can change and feel alright 我们能改变,我们能过的很好. I'm a little used to wandering outside the rain 有点习惯在雨中漫步 You can leave me tomorrow if it suits you just the same 如果你觉得会日子会更好,你可以明天就弃我而去 But I don't know enough, I need someone who leaves the day 但,我始终不解,我需要那个离开的人. Hey yeah 嘿耶 Cause it's hard for me to lose 因为我很少失败 In my life I've found only time will tell 我发觉在我的生活中只有时间才能证明一切 And I will figure out that we can baby 我坚信我们行的,宝贝 We can do a one night stand, yeah 我们可以享受一夜露水之欢 And it's hard for me to lose in my life 我很少失败 I've found outside your skin right near the fire 我从你的热情的外表上看到我们能行 That we can baby 我们行的,宝贝 We can change and feel alright 我们能改变,我们能很好的. Cause it's hard for me to lose 因为我很少失败 In my life I've found only time will tell 我发觉在我的生活中只有时间才能证明一切 And I will figure out that we can baby 我坚信我们行的,宝贝 We can do a one night stand, yeah 我们可以享受一夜露水之欢 And it's hard for me to lose in my life 我很少失败 I've found outside your skin right near the fire 我从你的热情的外表上看到我们能行 That we can baby 我们行的,宝贝 We can change and feel alright 我们能改变,我们能很好的. Cause it's hard for me to lose 因为我很少失败 In my life I've found only time will tell 我发觉在我的生活中只有时间才能证明一切 And I will figure out that we can baby 我坚信我们行的,宝贝 We can do a one night stand, yeah 我们可以享受一夜露水之欢 And it's hard for me to lose in my life 我很少失败 I've found outside your skin right near the fire 我从你的热情的外表上看到我们能行 That we can baby 我们行的,宝贝 We can change and feel alright 我们能改变,我们能过很好.