The prospects of Jerusalem artichoke in functional food ingredients and bioenergy production

12 Pages·2015·1.03 MB·English

by  Quan Sophia He

BiotechnologyReports5(2015)77–88
ContentslistsavailableatScienceDirect
Biotechnology Reports
journal homepage: www.elsevier.com/locate/btre
Review
TheprospectsofJerusalemartichokeinfunctionalfoodingredientsand
bioenergy production
Linxi Yanga, Quan Sophia Hea,*, Kenneth Corscaddena, Chibuike C. Udenigweb
aDepartmentofEngineering,FacultyofAgriculture,DalhousieUniversity,Truro,NSB2N5E3,Canada
bDepartmentofEnvironmentalSciences,FacultyofAgriculture,DalhousieUniversity,Truro,NSB2N5E3,Canada
ARTICLE INFO ABSTRACT
Articlehistory: Jerusalem artichoke, a native plant to North America has recently been recognized as a promising
Received17September2014 biomassforbioeconomydevelopment,withanumberofadvantagesoverconventionalcropssuchaslow
Receivedinrevisedform24November2014 inputcultivation,highcropyield,wideadaptationtoclimaticandsoilconditionsandstrongresistanceto
Accepted8December2014
pestsandplantdiseases.AvarietyofbioproductscanbederivedfromJerusalemartichoke,including
Availableonline13December2014
inulin,fructose,naturalfungicides,antioxidantandbioethanol.Thispaperprovidesanoverviewofthe
cultivationofJerusalemartichoke,derivationofbioproductsandapplicableproductiontechnologies,
Keywords:
withanexpectationtodrawmoreattentiononthisvaluablecropforitsapplicationsasbiofuel,functional
Jerusalemartichoke
foodandbioactiveingredientsources.
Functionalfood
ã2014TheAuthors.PublishedbyElsevierB.V.ThisisanopenaccessarticleundertheCCBY-NC-ND
Lacticacid
Bioactiveingredients license(http://creativecommons.org/licenses/by-nc-nd/3.0/).
Bioethanol
Biobutanol
Contents
1. Introduction ....................................................................................................... 77
2. CharacteristicsofJerusalemartichoke .................................................................................. 2
3. CultivationofJerusalemartichoke ..................................................................................... 2
4. BioproductsderivedfromJerusalemartichoke ........................................................................... 3
4.1. Functionalfoods .............................................................................................. 3
4.1.1. Inulin ................................................................................................ 3
4.1.2. Fructose .............................................................................................. 4
4.2. Bioactivecompounds .......................................................................................... 5
4.3. Biofuels ..................................................................................................... 5
4.3.1. Ethanol .............................................................................................. 5
4.4. Separatehydrolysisandfermentation ............................................................................. 6
4.5. Simultaneoussaccharificationandfermentation .................................................................... 6
4.5.1. Butanol .............................................................................................. 8
4.6. Chemicals ................................................................................................... 8
5. Conclusions ........................................................................................................ 8
Acknowledgement .................................................................................................. 9
References ........................................................................................................ 9
1.Introduction
Since the beginningof the 21st century, civilizationhas been
facingtwomajorproblems:thesteadydeclineoffossilfuels,and
environmentalproblemscausedbytheextensiveuseofthesefossil
fuelsfortheproductionofenergyandchemicals.Oneeffectiveway
* Correspondingauthor.Tel.:[phone];fax:[phone].
toaddressthesechallengesistousebiomassinsteadoffossilfuels
E-mailaddress:[email protected](Q.S.He).
http://dx.doi.org/10.1016/j.btre.2014.12.004
2215-017X/ã2014TheAuthors.PublishedbyElsevierB.V.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/3.0/).
78 L.Yangetal./BiotechnologyReports5(2015)77–88
fortheproductionoffuelsandchemicals,anemergingareatermed hairy oval shaped leaves and an underground rhizome system
as“bioeconomy”.Thistypeofeconomyundoubtedlycontributesto whichbearssmalltubers.ItisanAngiospermplantspeciesofthe
environmental, social and economic sustainability if it is well Compositae family, which is commonly referred to as the
designedandimplemented[1–3].Acriticalaspectofshiftingfrom sunflower or daisy family [10,20–22]. The stems are stout and
thecurrent“petroeconomy”toa“bioeconomy”istominimizethe ridged which can become woody overtime. Its leaves alternate
impactofnewapplicationsofbiomass(i.e.,fuelsandchemicals)on nearthetopofthestem,thelowerleavesarelargerandbroader,
traditionalusesofbiomass(i.e.,foodandfeed),therebypreventing andcangrowupto30cmlongwhilethehigheronesaresmaller
anyresultanteconomicimbalance.Therefore,significantacademic andnarrower.Intermsofflowerheads,eachis5–7.5cmwideand
and industrial activities are focused on identifying abundant formed by small, yellow, tubular disk flowers in the center and
biomasssourcesand/ordevelopingcropsthatarelesscompetitive surroundedbyflorets,whichoccurseparatelyoringroupsatthe
with conventional crops in terms of water, land and nutrient endofalarbranchesandmainstems.Asfortubers,theyareuneven
requirements.Theavailabilityandapplicationofbiomasssources andelongatevaryingfromknobbytoroundclusters.Thecolorsof
areregion-dependentanditisthereforeessentialtoidentifyplant tubersrangefrompalebrowntowhite,redandpurple[10,23].The
species suitable to local cultivation conditions to increase the morphologyofJerusalemartichokeplantandtubersareillustrated
economic viability of biomass production [4–6]. Two commonly inFig.2.
cited examples of successful transition to a bioeconomy include The Jerusalem artichoke was first cultivated by Native
bioethanol production from sugarcane in Brazil and biodiesel Americans long before the arrival of the Europeans, and was
production from non-edible Jatropha oil in South Asia; however, calledsunroots.FollowingitsintroductiontoEurope,diverseLatin
thesespeciescannotbeappliedreadilytoNorthAmericawithout and common names were ascribed to Jerusalem artichoke. Kays
consideringthedegreeofclimaticadaptation[7–9]. andNottingham[22] collectedandreportednearly100common
JerusalemartichokeisaplantnativetoNorthAmerica.Ithasa names used in different languages. Now some of the most
numberofadvantageouscharacteristicsovertraditionallyagricul- commonly used English names include Jerusalem artichoke,
tural crops, including high growth rate, good tolerance to frost, sunchoke, topinambur, woodland sunflower or earth apple.
droughtandpoorsoil,strongresistancetopestsandplantdiseases, Interestingly, the name “Jerusalem artichoke” is misleading as it
withminimaltozerofertilizerrequirements[10,11].Convention- isatypeofsunflowerinthesamegenusasthegardensunflower;
ally, Jerusalem artichoke has been used for food or animal feed however, it has no relation to Jerusalem, neither is it a type of
[12,13],andforthepasttwodecades,alternativeuseshavebeen artichoke[24].
explored especially for the production of functional food ingre-
dientssuchasinulin,oligofructoseandfructose[14,15].Itisalso 3.CultivationofJerusalemartichoke
found that some bioactive ingredients can be extracted from its
leavesandstems,whichcreatesanopportunityforapplicationsin Jerusalem artichoke is native to temperate regions of North
the pharmaceutical sector[16,17]. Morerecently, a renewedand Americaandcantolerateanannualprecipitationrangingfrom31
rapidly growing interest is for the use of Jerusalem artichoke to282cm,withsuitableaveragetemperaturerangeof6.3–26.6(cid:1)C,
tubers, which are rich in inulin, as raw materials for bioethanol andpHof4.5–8.2.Althoughitcanadaptwelltoawiderangeofsoil
production [18,19]. Multiple applications of Jerusalem artichoke typesandpHlevelsinasunnyposition,slightlyalkalinesoilsare
areillustratedinFig.1.Thesediverseapplicationsalongwithlow- favorableforartichokeproduction.Generallytheplantcantolerate
costofplantationrenderJerusalemartichokeapromisingbiomass sub-zerotemperatureswhilethetuberscanwithstandfreezingfor
forthedevelopmentofabioeconomy. several months even if the frost kills the stems and leaves. The
This review is a comprehensive survey of the cultivation of cold-tolerantnatureofthetubersallowsthemtobepreservedin
Jerusalem artichoke, production of a variety of potential bio- the ground during the cold winter until harvested as required
products and applicable production technologies. Considerable [10,22].
emphasisisplacedonJerusalemartichokebioethanolproduction. Several studies suggested that Jerusalem artichoke should be
plantedinearlyspringtoadepthof10–15cm.Seedtubersshould
2.CharacteristicsofJerusalemartichoke bespaced30–60cmapartineachrow,withrows45–120cmapart.
The optimal soil temperature for planting is between 6 and 7(cid:1)C
Jerusalemartichoke(Helianthustuberosus)isaperennialplant duetothefactthattubersbecomedormantattemperatureslower
which consists of a stemabout 1–3m tall, small yellow flowers, than 5(cid:1)C. Ideally, it should be planted in well-drained soil with
[(Fig._1)TD$FIG]
Fig.1. MultipleapplicationsofJerusalemartichoke.
[(Fig._2)TD$FIG] L.Yangetal./BiotechnologyReports5(2015)77–88 79
Fig.2. PlantandtubersofJerusalemartichoke.
slightalkalinity.ThesuggestedvalueofsoilpHforgrowthranges inulin, oligofructose and fructose [10,22,31,32], having both
from4.5to8.2.Irrigationisnotnormallyneededandtheplantis nutritional and functional attributes, particularly beneficial to
usuallyreadytobeharvestedinapproximately125days.Yieldsare individualswithType2diabetesandobesity[33–35].
relatively high, typically 16–20t/ha for tubers, and 18–28t/ha
green weight for foliage. It can be harvested using potato 4.1.1.Inulin
harvesting machinery. Once harvested, it needs to be handled Inulinisapolysaccharide,similartostarch,andexistsasawhite
carefullytopreventbruising.Recommendedstorageconditionsare powderwithneutraltaste.Chemically,itisalinearbiopolymerof
0–2(cid:1)Catarelativehumidityof95%for4–5months[10,13,25,26]. D-fructose units connected by b (2,1) glycosidic linkages, and
TheJerusalemartichokehasanaggressivenessnatureandshould terminated with one D-glucose molecule linked to the fructose
a
be managed cautiously with tubers missed during harvest chainbyan (2,1)bond.Thedegreeofpolymerizationofinulin
expected to grow aggressively in next season. However, this generallyrangesfrom2to60.Todate,inulinhasbeenincreasingly
aggressivenatureisadvantageousandreducestheneedforpest usedasfunctionalingredientsinprocessedfoodsduetoitsunique
managementsincetheplantgrowssoquickly[13,27]. characteristics[10,36,37].
b
DuetothepotentialapplicationofJerusalemartichokeinthe Inulinwiththe (2,1)linkagesbetweenthefructosemonomers
bioenergysector,itisnowincreasinglygrownasaspecialtyplant cannot be digested by human intestinal enzymes, giving rise to
by many farmers. Although aggressive growth is expected, for important applications in functional foods suitable for manage-
commercialscalecultivation,itstillmaybenecessarytoidentify ment of Type 2 diabetes, obesity and other blood sugar-related
regional pests and diseases that may affect crop growth. healthconditions[33,36–39].Whenorallyingested,inulinpasses
Unfortunately very little research is reported on this aspect. through the mouth, stomach and small intestine without being
McCarter and Kays [28] found that rust and powdery mildew metabolized, until it enters into the large intestine where it
caused by Puccinia helianthi and Erysiphe cichoracearum, respec- becomesfermentedbythecolonicmicroflora.Thus,consumption
tivelyreducedthetuberyield.Otherpotentialissuessuchasslugs, ofinulinhasnoinfluenceonbloodsugarlevelsandstimulationof
birds, deer and rabbits may pose a threat to the plant, as do insulin secretion. The non-digestible nature of inulin inherently
diseasessuchaspowderymildewandSclerotiniarot[13,29]. results in a caloric value that is significantly lower than other
typical carbohydrates, since energy is only derived from the
4.BioproductsderivedfromJerusalemartichoke metabolismoffattyacidsandlactateresultingfromfermentation.
Consequently,inulincanbeusedtoreplacefat,sugarandflourin
4.1.Functionalfoods dairyproducts,incerealsandinbakedgoodsforcaloriereduction
[40–42].Additionally,inulinisconsideredaformofsolubledietary
A functional food is defined as food that is demonstrated to fiberandiscategorizedasaprebiotic.Inulininfluencesintestinal
affect at least one target function in the body beyond basic functions by increasing stool frequency and stool amounts,
nutritionaleffects,inawaytoeitherenhancestageofwell-being particularly in constipated patients, along with decreasing fecal
and health and/or reduce the risk of disease. A functional food pHvalue.Theseeffectshelpsuppresstheproductionofputrefac-
mustremaininanormalfoodformratherthanpillsorcapsules, tivesubstanceinthecolon[33,37,43–45].Inulinasaprebioticalso
anddemonstratetheireffectsinamountsthatcanbeconsumedin simulatesthegrowthofexistingstrainsofbeneficialbacteriainthe
thediet.Afunctionalfoodcanbeanaturalfood,orafoodwhich colon which enhances the absorption of important mineral
oneormorecomponentshavebeenaddedto,orremovedfrom,or componentslikecalciumandmagnesiumaswellasthesynthesis
afoodwherethenature/bioavailabilityofoneormorecomponents of B vitamins [33,36,46–49]. It was also found that the incorpo-
has been modified, or any combination of these possibilities rationofinulininadietreducedthelipidcontentofbloodandliver
[30,31]. Jerusalem artichoke is a natural raw material for the insaturatedfat-fedrats.However,similareffectshavenotyetbeen
derivation of a number of functional food ingredients such as confirmedinhumans[50–53].Recentstudiesobservedthatinulin
80 L.Yangetal./BiotechnologyReports5(2015)77–88
played an important role in the prevention and inhibition of ofadvantages,includinghigheryields,lessdegradationofinulin,
colorectal,colonandbreastcancers[37,54–58]. room temperature operation and much less amounts of water
Oligofructose, another functional ingredient, is a short chain used.
polysaccharide containing less fructose units (2–10). It can be
derived from partial hydrolysis of inulin. Oligofructose has very 4.1.2.Fructose
similar functional and nutritional properties as inulin Inulincanbecompletelyhydrolyzedtoitsmonomer,fructose,
[31,33,37,42,44,59,60] and its applications as a functional food whichiswidelyusedassweetenerinsteadofsucroseorglucosein
ingredientarenotrepeatedlystatedinthispaper. functional foods, pharmaceuticals and beverages. The most
Giventhesehealthbenefitsofinulin,thedevelopmentofmore significant difference between fructose and other monosacchar-
efficientprocessesforinulinproductionandfeedstockidentifica- idesisthedifferenceinglycemicindex(GI).GIwasfirstintroduced
tionhavegainedconsiderableattention.Jerusalemartichokeand by Jenkins et al. [70] as a means to categorize carbohydrates
Chicory are the two most commonly used sources for inulin accordingtotheirabilitytoraisebloodglucose,andhasbeenused
productiononanindustrialscale[37].Jerusalemartichoketubers to help individuals with Type 2 diabetes and obesity with their
containahighamountofmedium-lengthchainsofinulinthatcan foodselection.Basedonthisdefinition[70],GIisdeterminedby
be extracted by the processes similar to sugar extraction from measuring the blood glucose response caused by ingestion of a
sugarcane. A typical inulin production process includes three certain amount of carbohydrate with respect to a rise in blood
majorsteps,namelypretreatment,extractionandpurification.In glucosecausedbythesameamountofglucoseintake.GIofglucose
ordertoincreasediffusionrate,Jerusalemartichoketubersarefirst isassumedas100,andGIofsucroseis65whileGIoffructoseis
sliced and ground into small particles. Extraction usually is only23[71].ThesignificantlylowGIoffructosemakesitthemost
conductedinhotwater.Followingseparationfromsolidresidues, favorable sweetener for patients with diabetes or obesity
inulinandwatersolutionisfurtherpurifiedbybleaching,activated [34,35,72]. More interestingly, the sweetness of fructose was
carbonadsorptionorion-exchangeapproaches.Purifiedinulinin reported to be 100–150% higher than that of sucrose, which
wateristhenconcentratedanddriedtogivefinishedpureinulin indicatesthatusingasmalleramountoffructosecanprovidethe
powders [61]. Even though an inulin production process is not same texture and sweetness in food than obtained using other
complicated, it is still challenging to obtain inulin with good sugars [73–76]. Less sugar intake definitely helps reduce the
quality and high yield. Therefore, efforts made to increase the microbialdecompositionandaggregationinthemouthleadingto
economic viability of inulin production are hereby briefly lowerchanceoftoothdecay.Thereforeitisextremelyattractiveas
reviewed. fructose additive, not only satisfies the taste buds, but also
Jerusalemartichoketuberscontainakindofenzymeexistingin producesrelevanthealthbenefits.
their epidermal cells, called polyphenol oxidase (PPO). Once Conventionally,fructoseisproducedfromhydrolysisofstarch,
harvested,tubersarestillengagedinaseriesofphysiologicaland involvingthree enzymesamylases oralpha-amylase andglucoa-
metabolicactivities.PPOcanoxidizetheendogenouspolyphenols mylaseinthreestepswhiletheresultinghydrolysatecontains45%
intomelanininthepresenceofoxygen.Thisprocessisknownas fructose and 55% glucose [77,78]. Inulin is a more advantageous
browning,whichseriouslyaffectthenutrient,flavorandappear- feedstockthanstarchsincehydrolysisofinulinneedsonlysingle
anceofthefinishedproduct.Li[62]systematicallyinvestigatedthe enzymatic hydrolysis with inulinase as biocatalyst [79], with
effects of temperature and pH value on the activity of PPO, and fructose yields reported as high as 95% [77]. The economy of a
suggestedthatapretreatmentofJerusalemartichokeinwaterwith hydrolysis process is highly associated with the activity and
aneutralpHvalueat80(cid:1)Cfor2minsuppressedenzymeactivity, stabilityofenzyme,operatingmodeandbioreactorconfiguration.
and thuseffectivelyeliminatedthe occurrence of browning.In a Comparedtomostchemicalreactions,biologicalreactionssuchas
studyconductedbyJiang[63],theeffectsofextractionoperating hydrolysisarerelativelyslow.Itrequiresalongreactiontimeorthe
parameters on the yield of inulin were evaluated, and optimal use of large bioreactors. In addition, large amounts of enzyme
extractionconditionsforachievinganinulinyieldof89.5%were involvedinhydrolysisremaininreactionbrothafterthereaction
provided: extraction temperature of 70(cid:1)C, ratio of water to andareverydifficulttorecover.Therefore,significantresearchhas
Jerusalem artichoke solid of 15:1, extraction time of 90min and been conducted to immobilize the enzyme to retain biocatalyst
two times of re-extraction of solid residues. Kierstan [64] andatthesametimetoachievecontinuousoperation.Riccaetal.
attemptedanenzymaticmethodtoisolateinulinfromJerusalem [80] have reviewed the main advancements achieved in the
artichoke, expecting an increased inulin yield. However their production of fructosefrom inulin enzymatic hydrolysisprior to
research indicated that enzyme treatment of crude Jerusalem 2007. Progress made in recent years or research not covered in
artichoke had no significant improvement on the extraction Ricca's review is summarized here with a focus on newenzyme
efficiency and the best extraction method required the involve- development, enzyme immobilization and innovative bioreactor
ment of some mechanical means. Sonication is increasingly design.
employed in solvent extraction of bioactive ingredients from ResearchconductedbySirisansaneeyakul,etal.[81]focusedon
vegetablesasitiscapableofenhancingmasstransferandsolvent the synergistic effect of a combined exo- and endo-inulinases
penetration [65]. Research [66] conducted regarding the perfor- system.Theyobservedthatanenzymesystemconsistedofmold
mancecomparisonamongconventionalextraction,directsonica- andyeastinulinaseswithamixingratioof5:1,wasbetteratinulin
tion extraction and indirect sonication extraction found that hydrolysisthanthemoldandyeastalone.Theresultinghydroly-
indirect sonication extractionwas the most suitable method for satecontained78.2%offructose.Yuetal.[82]developedanovel
inulin extraction from Jerusalem artichoke. Microwave-assisted recombinantinulinase-secretingSaccharomycescerevisiaestrainto
extraction is another promising method to improve extraction produce glucose-free fructose from Jerusalem artichoke. Such a
efficiency [67]. Xiao et al. [68] applied a microwave-assisted recombinant biocatalyst was capable of hydrolyzing inulin into
extractionprocessininulinisolation.Theyobservedthatwiththe fructoseandglucose,andsubsequentlymetabolizingglucose.Asa
aidofmicrowaves,theyieldofinulinwasincreasedfrom10.8%to result, only fructose accumulated in the hydrolysate, which
12.2%onawetbasiswhiletheextractiontimewasdecreasedfrom provided a promisingone-stepprocesstoproducefructosewith
100min to just 6min. Zhu’s group [69] employed a three-stage highpurity.Guiraudetal.[83]attemptedtoimmobilizeinulinase
homogenateextractionforinulinpreparation.Incomparisonwith on a DEAE-cellulose matrix by a simple adsorption method. As-
theconventionalhotwaterextraction,thisprocesshadanumber preparedcatalystwastestedinacontinuousreactorataflowrate
L.Yangetal./BiotechnologyReports5(2015)77–88 81
of10mL/h,inulinsolutionof5g/L,at40(cid:1)Cfor3weeks,achievinga extracts of Jerusalem artichoke leaves presented the strongest
conversionrateforinulinof100%.InastudyconductedbySanta inhibitoryabilityforpeppergraymoldwithintheirexperimental
etal.[84],anovelsol-gelimmobilizingmethodwasemployedto scope.InmorerecentresearchconductedbyChenetal.[98] six
depositinulinaseonaporoussilicaxerogelmatrix.Thisbiocatalyst phenolicacidswereisolatedfromJerusalemartichokeleavesusing
presented a promising operational stability at 40(cid:1)C for 20 n-butanolasasolvent,andamongthesixphenolicacidsisolated,
consecutive24-hbatchrunswithoutnoticeabledecayinproduct caffeicacid,3,4-dicaffeoylquinicacidand1,5-dicaffeoylquinicacid
yield.Singhetal.[85]developedastablecontinuousflowreactor wereidentifiedtoberesponsibleforG.zeaeinhibition.Thisstudy
withinulinaseimmobilizedonDuoliteA568tohydrolyzeinulin. sufficiently demonstrates that Jerusalem artichoke leaves are a
Thereactorcouldruncontinuouslyataflowrateof4mL/h,at55(cid:1)C potentialsourceofnaturalfungicides.
for75daysandtheexperimentalhalf-lifewas72days,whichisa Conventional solvent extraction has been a major extraction
veryencouragingadvanceinthecontinuoushydrolysisofinulin. technology for the separation of bioactive ingredients from
Zhu’s group [86,87] has conductedongoingresearchon fructose Jerusalemartichokeleaves.Sincetheleavescontainawidevariety
productionfromJerusalemartichokesincetheearly1990s[86].An ofchemicalcompounds,extractsusingdifferentsolventswithout
innovativedynamicmembraneseparatorwasdevelopedandwas furtherpurificationshowedvaryingbioactivities[96–98].There-
coupledtoahydrolysisreactor,whichwasabletoperformreaction fore further work is needed to extract bioactive substances,
and separation at the same time. The enzyme was filtered by subsequently separate extracts, identify and characterize the
membrane spectator and recycled into the hydrolysis reactor bioactivityofeachcompound.Thereleaseofbioactivecompounds
providing a cost-effective process for fructose production. This from Jerusalem artichoke can be affected by processing. For
uniquedesignhasbeenappliedonanindustrialscale. instance,puffingandextrusionprocesseswererecentlyfoundto
increasethetotalphenoliccontent,freeradicalscavengingactivity
4.2.Bioactivecompounds andferricreducingantioxidantpowerofJerusalemartichoketea
infusion compared to processing by roasting and hot air drying
In addition to functional foods derived from Jerusalem [99]. Moreover, a previous study showed that a combination of
artichoke tubers, the leaves also have important applications. high hydrostatic pressure (HPP) and enzymatic treatments and
Jerusalemartichokeleavesaretraditionallyusedasafolkmedicine fermentationincreasedthephenoliccontentandinvitroantioxi-
forthetreatmentofbonefractures,skinwounds,swellingandpain dant (radical scavenging and superoxide-like) activities of
[88–90].Anumberofvaluablebioactivecompoundsofmedicinal Jerusalem artichoke tuber extract compared to water extraction
significancehavebeenisolatedfromtheaerialpartsofJerusalem [100]. Therefore, for industry scale production of bioactive
artichoke, demonstrating antifungal, antioxidant, anticancer ac- compounds from Jerusalem artichoke, processing and extraction
tivitiesandothermedicinaleffects[16,17,88,91–98]. technologyshouldbecriticallyevaluatedandselectedaccordingto
InresearchconductedbyNakagawaetal.[92],twolectinswere the physicochemical properties of targeted ingredients and the
extractedfromcallusofJerusalemartichoke,andthenpurifiedby nature of the plant matrix. In addition to HPP, other non-
chromatography and preparative electrophoresis. Both lectins conventional extraction techniques such as ultrasound-assisted,
showed a strong activity for hemagglutination. Pan et al. [16] microwave-assisted and supercritical fluid extraction can be
successfully isolated nine bioactive compounds from the whole considered as alternative approaches to increase the yield and
plantofJerusalemartichoke,includingent-17-oxokaur-15(16)-en- preserve the bioactivity of ingredients in Jerusalem artichoke
b
19-oic acid, ent-17-hydroxykaur-15(16)-en-19-oic acid, ent-15 - [101,102].
hydroxykaur-16(17)-en-19-oic acid methyl ester, ent-15-nor-14-
oxolabda-8(17), 12E-dien-18-oic acid, 4,15-isoatriplicolide ange- 4.3.Biofuels
late, 4,15-isoatriplicolide methylacrylate, (+)-pinoresinol,
((cid:3))-loliolide, and vanillin. The bioactivities of nine compounds 4.3.1.Ethanol
were subsequently evaluated using the MCF-7 human breast Jerusalemartichoke(JA)iscurrentlyrecognizedasanemerging
cancer cell line and a soybean isoflavonoid defense activation energycropforbioethanolproduction;however,ethanolproduc-
bioassay. Two of the compounds were identified as cytotoxic tion from Jerusalem artichoke has a long history. In the 19th
agents, one of which was capable of stimulating defense century, a French chemist, Anselme Payen promoted Jerusalem
metabolites, and four of which were able to block isoflavone artichoketubers for beerproductioninFrance.Interestingly,the
accumulationinsoybean.Continuouseffortsonbioactiveingredi- beerderivedfromJerusalemartichoketubersissweetandhasa
entextractionfromJerusalemartichokeleavesinXiaoandYuan’s fruity taste [103,104]. Due to the unique aroma, Jerusalem
team [17,93,94] have led to important advances. Six phenolic artichokeethanolhasalsobeenusedtoproducebrandyinFrance
extracts from Jerusalem artichoke leaves exhibited free radical andGermanyaswellassakeinJapan[105].DuringandafterWorld
scavengingactivities,renderingJerusalemartichokeleavesagood WarI,extensiveresearchwasconductedbytheBritishDepartment
source for natural antioxidants [17,95]. Very recently, this group ofScientificandIndustrialResearchtodevelopfuelethanolfrom
[94]furtherisolatedaseriesofsesquiterpenelactones,exhibiting Jerusalemartichoke.ItwasdemonstratedthatJerusalemartichoke
cytotoxicityagainstcancercelllines,whichisconsistentwiththe wasabletoproducethesameamountoffermentablecarbohydrate
resultsreportedbyPanetal.[16]. peracreforalcoholassugarbeetandmorethantheIrishpotato.
The extracts from Jerusalem artichoke leaves also exhibited However,withtheriseofthemodernpetroleumindustry,interest
antifungalproperties[96–98].Liuetal.[96]useddifferentsolvents infuelethanoldeclined[106,107].Inthe1980sarenewedinterest
to extract Jerusalem artichoke leaves, and tested extracts’ inJerusalemartichokeethanolwasstimulatedbythe1973oilcrisis
antifungal properties in several fungi such as Rhizoctonia solani, [108,109];howeverthisresearchwasagaininterruptedwithlower
Gibberella zeae, Alternaria solani and Botrytis cinerea. Their study oil prices following the crisis. Renewed interest in Jerusalem
indicated that Jerusalem artichoke leaf extracts from different artichoke as a source for ethanol production has occurred again
solvents showed different antifungal activities. For example, the and this time is largely driven by the rapid decline of fossil fuel
inhibitoryeffect of aqueous extracts was lower than those from reservescoupledwiththenegativeeffectsofoverconsumptionof
organic solvents. The extracts from ethyl acetate showed the petroleum-based fuels on environment such as global warming,
highest inhibitory activity to the four fungi employed in this climatechange,acidrainandozonelayerdepletion.Mucheffort
research.WhileastudyfromHanetal.[97]foundthattheacetone and significant progress have been made to develop biofuels,
82 L.Yangetal./BiotechnologyReports5(2015)77–88
mainlybioethanolandbiodieseltosubstitutepetro-fuels[110,111]. yield.ItwasalsoobservedthatZ.mobiliswasabletofermentthe
CurrentlyinNorthAmerica,corn,wheatandbarleyaredominant Jerusalem artichoke juiceintoethanol without adding anyother
feedstocks for commercial bioethanol production but they nutrients, and the ethanol yield using Z. mobilis in fermentation
compete with food and feed supply, raising a heated debate on washigherthanfoundusingK.marxianus.KimandHamdy[125]
“fuelvsfood”.Asaconsequence,effortsarereorientedtoutilize optimizedhydrolysisconditionstoobtaincompletehydrolysisof
lignocellulosicbiomass(agriculturalandforestryresidues)and/or inulinandminimumgenerationofyeastinhibitors.Theyproposed
develop dedicated energycrops [1,112–115]. Undoubtedly, ligno- thatJerusalemartichokeslurryshouldbehydrolyzedin0.1MHCl
cellulose is the most economical and abundantly available at97(cid:1)Cfor15min.Undersuchconditions,maximumreductionof
feedstock,howeverthecostlypretreatmentofconvertingcellulose sugar to 84.8% fructose equivalent was achieved while the
intofermentablesugaristhekeytechnicalbarriertoeconomically concentration of inhibitor 5-hydroxymethylfurfural (HMF) was
competitive production. Bioethanol production from lignocellu- 0.07%, lower than 0.1%, the limit for yeast growth inhibition.
losic biomass is still at the development stage [116]. Jerusalem Razmovski et al. [126] examined the effects of temperature,
artichoketubersarerichininulin,whichcanbeeasilyhydrolyzed residencetimeandhydromoduleonJerusalemartichokehydroly-
and then converted into ethanol using biocatalysts. The ethanol sis.TheJerusalemartichokehydrolyzatesobtainedundervarious
yield is equivalent to that of sugarcane and twice that obtained hydrolysisconditionswerefurthertestedinalcoholicfermentation
from corn. These characteristics make Jerusalem artichoke an withS.cerevisiaeasabiocatalyst.Theyfoundthatacidhydrolysis
outstandingsubstrateforethanolproduction[18,19,117–119],and at high temperatures and long residence times increased
it has recently been listed as one of the most promising energy the concentration of yeast inhibitor HMF and accelerated the
crops in China, Europe and New Zealand [4,120–122]. Generally, degradation of fructan. Based on their experimental results, the
there are two routes for bioethanol production from Jerusalem highestethanolyieldof7.6w/wwasobtainedwhenacidhydrolysis
artichoketubers:(1)separatehydrolysisandfermentation(SHF) was carried out at 126(cid:1)C, 60min of residence time and hydro-
and (2) simultaneous saccharification and fermentation (SSF) as moduleratioof1:1.Zubr[127]investigatedtheeffectsofseveral
showninFig.3. enzymes on hydrolysis of Jerusalem artichoke tubers, including
Novozym 188, Celluclast, Novo 230, Novo SP 249, and combina-
4.4.Separatehydrolysisandfermentation tionsofthereof.Theirworkindicatedthatcellulolyticenzymeslike
Novozym 188 and Cellules had very disappointing performance,
Separatehydrolysisandfermentation(SHF)methodischarac- generatingasmallamountoffructoseandglucose.Novo230was
terized as inulin hydrolysis and sugar fermentation being themostefficientenzymeforinulinhydrolysis,givingthehighest
conductedintwoseparatereactors.Typically,Jerusalemartichoke sugar yield under the authors’ experimental scope. At the same
tubers are processed into pulpy mash and then hydrolyzed into time, S. cerevisae, traditional brewing yeast, was identified as an
fermentable sugars (fructose and glucose) using either dilute efficientcatalystforthealcoholicfermentationoftheseferment-
mineral acids or inulinase enzyme. Subsequently, fermentable ablesugarsresultedfromhydrolysisstep.
sugar is separated from solid residues and transferred into a
fermenterwheresugarisfermentedintoethanolemployingyeasts 4.5.Simultaneoussaccharificationandfermentation
suchasZymomonasmobilis,KluyveromycesmarxianusandSaccha-
romycescerevisae. Simultaneoussaccharificationandfermentation(SSF)ischar-
Theresearchonhydrolysisofinulinforfructoseproductionhas acterizedasinulinhydrolysisandsugarfermentationbeingcarried
beenstatedinSection4.1.2.[77–87]Such-preparedfructosecanbe out in one bioreactor using combination biocatalysts. Obviously,
furtherconvertedintoethanol.Fortheethanolproductionstarting suchadirectconversionofsolubleinulinintoethanolwithouta
with tubers through SHF process, hydrolysis step has significant prior hydrolysis step is highlyfavorable from capital investment
impactsonthefollowingfermentationstep.Completehydrolysis and operating cost perspectives. Moreover, a SSF process
ofinulinproducesamaximumamountofsugarthatleadstohigh significantly reduces the fermentable sugar loss caused by
ethanol yield. However, hydrolysis process may generate some separationandtransferofsugarsfromhydrolyzerintofermenter
byproducts which could inhibit the activity of yeast in the as in a SHF process. For Jerusalem artichoke ethanol production
fermentation step, consequently prolonging fermentation time. throughSSF,themajortechnicalbarrieristheidentificationofthe
Fleming et al. [123] investigated the effectiveness of various most efficient enzymes which are capable of facilitating both
mineralacids(hydrochloric,sulfuric,citricandphosphoricacids) hydrolysisandfermentation.
in hydrolysisofJerusalemartichoke tubers.Theyconcludedthat One approach is to use a mixture of inulinase and yeast to
there was no significant difference among these acids in their convert ground Jerusalem artichoke tubers to ethanol. Kim and
influenceoninulinhydrolysis.TheresearchconductedbyToran- Rhee [128] co-immoblized inulinase and Z. moblilis in alginate
Diazetal.[124]evaluatedtheeffectofacidorenzymatichydrolysis beadstofacilitateaone-stepproductionofethanolfromJerusalem
ofinulinonthesubsequentalcoholicfermentation.Itwasfound artichoke tubers in a continuous mode. The maximum ethanol
thatacidhydrolysiswasfasterthanenzymatichydrolysiswhilethe productivitywasreportedas55.1g/L/handtheyieldwas95%of
byproductsfromacidhydrolysisinhibitedthegrowthofyeastin theoretical yield. In the study reported by Nakamura et al.
thesubsequentfermentationstep,whichresultedinalowethanol [129,130], simultaneous hydrolysis and fermentation of tubers
[(Fig._3)TD$FIG]
Fig.3. TworoutesforbioethanolproductionfromJerusalemartichoketubers.
L.Yangetal./BiotechnologyReports5(2015)77–88 83
was conducted in a batch operation mode using a mixture of ethanol production. However, these processes involving two
Aspergillus niger 817 and S. cerevisiae 1200. The ethanol concen- species with different culture conditions pose difficulties to
trationwas10.4%(v/v)for15hfermentationtime;theyieldwas process optimization. Ethanol productivity was compromised
92% of theoretical yield. Szambelan et al. [131] compared the due to both biocatalysts working under sub-optimal conditions.
ethanol yields from different processes, using single yeast and a Another effort is to use yeasts that possess inulinase activity to
mixture culture of microorganisms. The mixed culture of achievesimultaneoussaccharificationandfermentation.Guiraud
KluyveromycesfragilisandZ.mobilisorK.fragilisandS.cerevisiae et al. [133] first demonstrated that K. fragilis and K. fragilis with
gavethebestresultsundertheauthors’researchscope.Theyieldof inulinaseactivitywereabletoconvertJerusalemartichoketubers
ethanol was 94% of maximum theoretical yield and the ethanol toethanoldirectly.Followingtheirpioneeringresearch,numerous
concentrationwas 9.9% (v/v). Ge et al. [132] attempted a newly effortsweremadetodevelopand/orscreenmoreeffectivestrains
isolated extroinulinase-hyperproducing strain, A. niger SL-09, tofacilitateSHFofJerusalemartichoke.Duvnjak[134] evaluated
coupled with S. cerevisiae Z-06 to ferment ground Jerusalem theperformanceofseveralyeastsinhydrolysisandfermentation,
artichoke tubers into ethanol in a batch operation. The ethanol including K. marxianus ATCC12708, K. marxianus ATCC 10,606,
concentrationwasashighas19.5%(v/v)for48hfermentationwith Kluyveromyces cerevisiae ATCC 22,295 and K. fragilis. Their work
theconversionefficiencyof90%.Theresultfromthisresearchis indicated that Jerusalem artichoke juice contained enough
significant in that high ethanol concentration in the finished nutrients for both yeast growth and ethanol production. K.
fermentation broth can dramatically reduce the cost of the marxianus ATCC12708 was identified as the most suitable yeast,
subsequent distillation step, making the overall ethanol produc- providinganethanolyieldof87.5%oftheoreticalvaluewithin25h
tionmoreeconomicallyviable. fermentation. From the early 1980s, Professor Margaritis’s team
Employmentofamixtureofenzymescanrealizesimultaneous [108,109,135–149] have been devoting their research to ethanol
hydrolysis and fermentation of Jerusalem artichoke tubers for production from Jerusalem artichoke. Extensive works were
Table1
SSFprocessesreportedinliterature.
Biocatalysts Fermentationconditions Ethanolconcentration Yielda Reference
Simultaneoussaccharificationandfermentation(SSF)
(amixtureofvariousenzymes)
Inulinase+Z.moblilis 35(cid:1)C,continuous 55.1g/L/h 95% Kim[128]1990
A.niger817+S.cerevisiae1200 30(cid:1)C,15h 10.4%(v/v) 92% Nakamuraetal.[130]
1996
K.fragilis+ 30(cid:1)C,72h 9.9%(v/v) 94% Szambelanetal.[131]
Z.moblilis3881 2005
K.fragilis+ 30(cid:1)C,72h 9.1%(v/v) 86%
S.cerevisiaeBc16a
A.nigerSL-09+ 30(cid:1)C,48h 19.6%(v/v) 90% GeandZhang[132]2005
S.cerevisiaeZ-06
Simultaneoussaccharificationandfermentation(SSF)
(yeastwithinulinaseactivity)
K.fragilis 28(cid:1)C,6days 11.1%(v/v) 98% Guiraudetal.[133]
1981
K.marxianus 28(cid:1)C,6days 11.5%(v/v) 98%
K.marxianusATCC12708 28(cid:1)C,30h 14g/L 87% Duvnjaketal.[134]
1981
K.marxianusATCC10606 28(cid:1)C,30h 12g/L 83%
K.cicerisporusATCC22295 28(cid:1)C,30h 13g/L 86%
K.fragilis105 28(cid:1)C,30h 11g/L 79%
K.marxianusUCD55-82 35(cid:1)C,60h 44g/L 88% BajpaiandMargaritis[138],
K.marxianusUCD55-82 35(cid:1)C,continuous 7g/L/h 90% Sachsetal.[106],
1982
K.marxianusCECT10875 28(cid:1)C,30h 19g/L 96% Negro[150],2006
K.cicerisporusY179 30(cid:1)C,144h 12.3%(v/v) 86.9 Yuetal.[152],2010
S.cerevisiaeKCCM50549 30(cid:1)C,36h 32.6g/L 70% Limetal.[151]2011
K.marxianusATCC8554 35(cid:1)C,84h 60.9g/L 87% Yuanetal.[153],2008
S.cerevisiae6525withclonedinulinasegene 35(cid:1)C,48h, 72.5g/L 85% Yuanetal.[155],2013
K.marxianuswithoverexpressedinulinasegene 35(cid:1)C,72h, 96.2g/L 93% Yuanetal.[156]2013
SaccharomycesspW0withexo-inulinasegene 28(cid:1)C,144h 12.5%(v/v) 62.5% Zhangetal.[157]2010
SaccharomycesspW0with18SrDNAintegrationofexo-inulinasegene 28(cid:1)C,120h 12.6%(v/v) 66% Yuanetal.[156]2011
SaccharomycesspW0withendo-inulinasegene 30(cid:1)C,120h 12.6%(v/v) 65% Lietal.[159]2013
K.marxianusPT-1 40(cid:1)C,84h 73.6g/L 90% Huetal.[160]2012
orS.cerevisiaeJZ1C 40(cid:1)C,84h 65.2g/L 79.7%
S.cerevisiaeDQ1 30(cid:1)C,72h 128.1g/L 73.5% Guoetal.[161]2013
a Ethanolyieldisthepercentageoftheoreticalyieldonthebasisoftotalsugarinfeedstock.
84 L.Yangetal./BiotechnologyReports5(2015)77–88
conductedrangingfromyeastscreening[135],enzymeimmobili- verypromising.Table1summarizesthebiocatalysts,fermentation
zation method [136,139–142], batch and continuous operation conditionsandethanolproductivitiesofavarietyofSSFprocesses
modes [106,141,177], kinetics of ethanol production forJerusalemartichokeethanolproductionreviewedinthispaper.
[136,138,142,143]andhydrolysisofinulin[146–149],whichbuilt
a valuable foundation for the research on Jerusalem artichoke 4.5.1.Butanol
ethanol. In their early work, K. marxianus UCD (FST) 55-82 was Biobutanolasanewgenerationofbiofuelhasrecentlydrawn
demonstratedtobethemostsuitableyeastforthefermentationof increasing attention due to its higher heating value and low
Jerusalem artichoke tubers among eight yeasts tested in their volatilityincomparisonwithbioethanol.Explorativeresearchon
investigation[135].K.marxianusUCD(FST)55-82withinulinase butanolproductionfromJerusalemartichokehasbeenconducted.
activity was further employed in a continuous bioreactor to SarchamiandRehmann[162]optimizedtheenzymatichydrolysis
hydrolyze and ferment Jerusalem artichoke juice, producing ofinulinfromJerusalemartichoke,andobtainedmaximuminulin
ethanol with a yield of 90% of theoretical value [108]. The conversionof94.5%undertheoptimalconditions(temperatureof
performanceofthisyeastwasalsotestedinabatchoperationfor 48(cid:1)C,pHof4.8,substrateconcentrationof60g/L,enzymeloading
ethanolproduction[108].Theethanolconcentrationwas44g/Lat of10units/gsubstrateandfermentationtimeof24h),producing
theendofafermentationtimeof60h,achievingayieldof88%of butanolof9.6g/L.Chenetal.[163]usedClostridiumacetobutylicum
the theoretical yield. Negro et al. [150] conducted a direct L7tohydrolyzeJerusalemartichokejuice.Itwasfoundthatwitha
fermentation of inulin using K. marxianus CECT 10,875. The starting sugar concentration of 62.87g/L,11.2g/L of butanol was
ethanolconcentrationwas19g/Lattheendoffermentation,witha producedfor60hoffermentation,andtheratioofbutanol,acetone
yieldof96%oftheoreticalyield.WorkbyLimetal.[151]identified andethanolwas0.64:0.29:0.05.
S. cerevisiae KCCM50549 as another promising yeast for SFH
process of Jerusalem artichoke tubers, giving a relatively high 4.6.Chemicals
ethanolconcentrationof36.2g/Landayieldof70%oftheoretical
valuewithin 30h. Ethanol produced from this yeast is 1.6 times Lactic acid is widely used in the food, pharmaceutical and
higherthanthatfromS.cerevisiaeNCY625.Yuetal.[152]noticed chemical industries, and it is an important building block for
that Kluyveromyces cicerisporus Y179 expressed a high level of synthesizing a variety of chemicals [164,165]. In response to an
inulinase activity, which was suitable for ethanol production by increasingdemandforlacticacid,Jerusalemartichokestandsout
SSHmethod.Theexperimentalresultsindicatedthatmoreethanol asalowcostrawmaterialforlacticacidproduction.Geetal.[165]
was produced by this yeast at 30(cid:1)C than at 37(cid:1)C or 42(cid:1)C. After first attempted to use mixed culture of A. niger SL-09 and
144hfermentation,ethanolwiththeconcentrationof12.3%(v/v) Lactobacillus sp to produce lactic acid from JA. In a SSF process,
was achieved, and the yield of ethanol was 86.9% of theoretical thehighestlacticacidconcentrationof120.5g/Lwasobtainedin
value.Dr.Bai’sgroup[153–156]haveconductedongoingresearch 36h of the fed-batch fermentation with a high conversion
on ethanol production from Jerusalem artichoke tubers using a efficiency of 94.5%. This group further enhanced the process by
consolidated bioprocessing (CBP) strategy which integrated introducingLactobacilluscaseiG-02,leadingtoanincreasedlactic
inulinase production, hydrolysis of inulin and ethanol fermenta- acidconcentrationof141.5g/L[166].ItwasreportedbyChoietal.
tion.IntheearlyworkconductedbyYuanetal.[153]K.marxianus that a direct lactic acid fermentation could be realized using
ATCC8554 were proven to have a good alcoholic fermentation Lactobacillusparacaseiwithoutapre-stepofinulinhydrolysis.The
abilityandhighinulinaseproductioncapacity.Employmentofthis lacticacidconcentrationwas92.5g/Landtheconversionefficiency
yeast converted Jerusalem artichoke tubers to ethanol directly, ofinulin-typesugarstolacticacidwas98%ofthetheoreticalyield
achieving an ethanol yield of 87% for fermentation time of 84h. [167].Daoetal.[168]developedapracticalandeconomicalwayto
Yuanetal.[155]furtherdevelopedanewrecombinantyeastthat produce lactic acid from JA. They used commercially available
containedcommerciallyavailableS.cerevisiae6525integratedby glucoamylase,glucoamylaseGA-LNewandPediococcusacidilactici
inulinase gene cloned from K. marxianus. Using this new yeast, DQ 2 to hydrolyze and ferment JA tubes. The lactic acid
ethanol concentration in broth was significantly increased to concentration of 111.5g/L was obtained. Another study on lactic
72.5g/Lattheendof48hfermentation,whileusingthehoststrain, acidproduction[169]conductedbyWangetal.usedthermophilic
S.cerevisiae6525alone,ethanolconcentrationwasonly67.0g/Lin Basilluscoagulansstrain.Theobtainedlacticacidwas134g/Lwitha
60h. Yuan et al. [156] also applied K. marxianus with over- starting sugar concentration of 140g/L. Research from Shi et al.
expression of inulinase gene in the fermentation of Jerusalem [170]focusedonthedevelopmentofefficientbioreactors.Afibrous
artichoketubers.Significantimprovementofethanolproductivity bed bioreactor with immobilized Lactococcus lactis significantly
was observed, detailed data of which are listed in Table 1. The improvetheoverallproductionefficiency,resultinginlacticacid
researchofDr.Chi’steam[157–159]focusedonthedevelopment concentrationof142g/Linafed-batchmodeoperation.
and application of Saccharomyces sp W0 with inulinase gene Jerusalemartichokealsohaspotentialforgeneratingavariety
expression in Jerusalem artichoke ethanol production. The exo- ofotherschemicals[164,171]suchasbutyricacid[172],citricacid
inulinase gene and endo-inulinase gene were integrated into [173], succinic acid [174], 2,3-butanediol [175,176] and sorbitol
Saccharomyces sp W0 respectively. Ethanol productivities using [177].Afewstudieshavebeenreported,ofwhichdetailsarenot
SaccharomycesspW0withandwithoutinulinasegeneexpression statedinthispaper.
aresummarizedinTable1.Huetal.[160]examinedtheactivitiesof
21newlyisolatedand65previouslyavailableS.cerevisiaestrainsin 5.Conclusions
directfermentation of Jerusalem artichoke throughconsolidated
bioprocessing(CBP).TheirworkidentifiedK.marxianusPT-1andS. Jerusalem artichoke is an economically important plant with
cerevisiae JZ1C as good thermo-tolerant strain candidates for advantages of low input cultivation, high crop yield and wide
Jerusalemartichokeethanolproduction.Undertheirexperimental adaptation to climatic and soil conditions. In addition to its
conditions, these two strains gave 90% and 79.7% of theoretical applicationsasfunctionalfoodandbioactiveingredientsources,it
ethanolyieldrespectivelyat40(cid:1)Cwithin84hfermentation.Very is recognized as a sustainable feedstock for biofuel production.
recently,Guoetal.[161] reportedanimprovedCBPprocessina Thesediverseeconomicvaluesidentifyitasapromisingbiomass
helicalribbonstirringbioreactorusingmutantyeast,S.cerevisiae for bioeconomy development. However, Jerusalem artichoke is
DQ1. The ethanol concentrationwas as high as 128g/L, which is currently underutilized. This paper provides a review of the
L.Yangetal./BiotechnologyReports5(2015)77–88 85
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