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Towa d Comp ehensi e Plan Mic obiome Resea ch
© 2020 Saikkonen, Nissinen and Helande .
Published e sion
Saikkonen, Ka i; Nissinen, Rii a; Helande , Ma jo
Saikkonen, K., Nissinen, R., & Helande , M. (2020). Towa d Comp ehensi e Plan Mic obiome
Resea ch. F on ie s in Ecology and E olu ion, 8, A icle 61.
h ps://doi.o g/10.3389/ e o.2020.00061
2020
PERSPECTIVE
published: 13 Ma ch 2020
doi: 10.3389/ e o.2020.00061
F on ie s in Ecology and E olu ion | www. on ie sin.o g 1Ma ch 2020 | Volume 8 | A icle 61
Edi ed by:
Anne Duplouy,
Lund Uni e si y, Sweden
Re iewed by:
A ne Weinhold,
F eie Uni e si ä Be lin, Ge many
Ra ael Soa es Co ea De Souza,
Campinas S a e Uni e si y, B azil
Desalegn W. E alo,
Ne he lands Ins i u e o Ecology
(NIOO-KNAW), Ne he lands
*Co espondence:
Ka i Saikkonen
[email p o ec ed]
Special y sec ion:
This a icle was submi ed o
Coe olu ion,
a sec ion o he jou nal
F on ie s in Ecology and E olu ion
Recei ed: 24 No embe 2019
Accep ed: 26 Feb ua y 2020
Published: 13 Ma ch 2020
Ci a ion:
Saikkonen K, Nissinen R and
Helande M (2020) Towa d
Comp ehensi e Plan Mic obiome
Resea ch. F on . Ecol. E ol. 8:61.
doi: 10.3389/ e o.2020.00061
Towa d Comp ehensi e Plan
Mic obiome Resea ch
Ka i Saikkonen1*, Rii a Nissinen2and Ma jo Helande 3
1Biodi e si y Uni , Uni e si y o Tu ku, Tu ku, Finland, 2Depa men o Biological and En i onmen al Science, Uni e si y o
Jy äskylä, Jy äskylä, Finland, 3Depa men o Biology, Uni e si y o Tu ku, Tu ku, Finland
Mic obes ha e d i en eco-e olu iona y adap a ions o ganizing biodi e si y om he
o igin o li e. They a e ubiqui ous and abundan , acili a ing he biochemical p ocesses
ha make Ea h habi able and shape ecosys em s uc u es, unc ions, and se ices.
Recen s udies e eal ha commensalis ic and bene icial mic obes associa ed wi h
wild and domes ica ed plan s may aid in es ablishing sus ainable ag icul u e o a
changing clima e. Howe e , de eloping mic obe-based bio echnologies and ecosys em
se ices equi es a ho ough unde s anding o he di e si y and complexi y o mic obial
in e ac ions wi h each o he and wi h highe o ganisms. We discuss he ho and blind
spo s in con empo a y esea ch on plan mic obiomes, and how he la es molecula
biological echniques and empi ical eco-e olu iona y app oaches could ele a e ou
pe cep ion o mic obe–plan in e ac ions h ough mul idisciplina y s udies.
Keywo ds: bac e ia, ungi, mic obiome, endophy es, pa hogens, sap obes, ecology, e olu ion
UBIQUITOUS MICROBES IN THE SPOTLIGHT
Recen ad ances in molecula mic obiology ha e e olu ionized he abili y o he scien i ic
communi y o unde s and and s udy he di e si y and unc ions o mic obes associa ed wi h
animals and plan s, leading o a ple ho a o ela ed li e a u e. A Web o Science sea ch (Janua y
23, 2020) using “mic obiome” o “mic obiome and plan ” as opic keywo ds p oduced 28,733
e e ences published, wi h 49 and 1,211 o he pape s anked as “ho ” and “highly ci ed.” Mo e han
99% o he pape s we e published a e 2010. These s udies a e la gely based on mass sequencing
o axonomic ma ke genes o bac e ia and ungi (communi y sequencing), and o lesse ex en ,
me agenomes o mic obial communi ies. Cu en ly, s udies elying on molecula me hodologies
domina e plan mic obiome li e a u e.
Today we know ha mic obes a e ubiqui ous and essen ial associa es o i ually all highe
o ganisms. Fo example, he mic obial cells colonizing he human body appea o be mo e
abundan as ou soma ic cells and con ain o e whelmingly mo e genes han ou human genome
(Gilbe e al., 2018). Simila ly, mic obes ha e been ound in i ually all plan s (Pa ida-Ma inez
and Heil, 2011), and a e known o hei immense signi icance e.g., as plan bene icial myco hizae
and endophy es. Pa hogens such as co ee us , lea bligh o ubbe , Panama disease o banana,
ches nu bligh , Du ch elm disease, and po a o bligh ha e been culp i s o g ea his o ical
con ulsions wi h social impac s (Schumann, 1991). His o ically he po a o bligh , he causal
agen o he I ish po a o amine causing he dea h by s a a ion o one million people and
o e seas emig a ion o a u he wo million people in he mid-1800s (Schumann, 1991), has been
pa icula ly in luen ial in he eme gence o ge m heo y and in shaping he concep ual model o
disease iangle (Schumann, 1991).
Saikkonen e al. Holis ic Phy obiome Resea ch
We p opose ha as mic obes associa ed wi h hei sha ed
hos plan s comp ise mul ipa i e en i ies, he heo ies o
hologenome e olu ion (Saikkonen e al., 2006; Zilbe -
Rosenbe g and Rosenbe g, 2008; Mo an and Sloan, 2015;
Vandenkoo nhuyse e al., 2015; Theis e al., 2016; Rosenbe g
and Zilbe -Rosenbe g, 2018) and he geog aphic mosaic o
coe olu ion (Thompson, 2005) p o ide usable amewo ks
o unde s and hese mic obial-plan in e ac ions and hei
impo ance o ecological, e olu iona y and gene ic p ocesses.
Simila ly o human and animal mic obiomes (Gilbe e al.,
2018), he majo i y o plan mic obiomes a e acqui ed om he
en i onmen o ansmi ed ho izon ally be ween indi iduals.
Howe e , in modula o ganisms (Chapman, 1981) cha ac e ized
by soma ic emb yogenesis, such as mos seed plan s, many
long-las ing mic obe-plan in e ac ions in ol e ei he e ical
o pseudo- e ical ansmission om hos plan o i s sexual
and/o ege a i e o sp ing (Wilkinson, 1997; Saikkonen e al.,
1998; Canka e al., 2005). Thus, plan mic obiomes p o ide
a pa icula ly e ile g ound o ecologis s and e olu iona y
biologis s in e es ed in all le els o selec ion in co-e olu iona y
p ocesses. The use o me agenomic ools allow us o de e mine
he di e si y o mic obiomes and he “-omics” app oaches
(genomics, p o eomics and me abolomics) can be used o
examine how genomic in o ma ion is ansla ed in o s uc u es
and unc ions in he in e ac ions among plan and i s mic obial
pa ne s (Delmo e e al., 2009; Lundbe g e al., 2012; Sessi sch
e al., 2012; Ha doim e al., 2015; Agle e al., 2016; Saikkonen
e al., 2016; an de Heijden and Ha mann, 2016).
Fu he mo e, i we ake in o accoun ha pheno ypic selec ion
may ea he plan and i s associa ed mic obes indi idually o in
conce as a pheno ypic and me agenomic uni , he implica ions
o concep ions o gene ics, epigene ics (Jaenisch and Bi d, 2003;
Zilbe -Rosenbe g and Rosenbe g, 2008; Vannie e al., 2015) and
na u al selec ion a e p o ound. The nex s ep owa d a be e
unde s anding o he di e se oles o mic obiomes is o combine
me agenomic su eys ega ding he composi ion and unc ion
o mic obiomes wi h empi ical and heo e ical biological
app oaches including ecology, physiology, gene ics and
epigene ics, pheno ypic e olu ion, and coe olu ion o in e ac ing
species (Saikkonen e al., 2004, 2016; P osse e al., 2007;
Vandenkoo nhuyse e al., 2015; Vannie e al., 2015; Rosenbe g
and Zilbe -Rosenbe g, 2016; an O e beek and Saikkonen,
2016). This equi es he acknowledgmen and b eaking o ce ain
ba ie s and challenges associa ed wi h scien i ic adi ions and
managemen o inc easing in o ma ion o e load.
WHY INTERDISCIPLINARY
COLLABORATION IS NEEDED
We con end ha human pe spec i e o en hampe s
unde s anding o he complex na u e o mic obe–plan
in e ac ions and hei impo ance o ecosys em unc ions
and se ices. Con en ional wisdom biased by human
pe cep ions migh misdi ec scien i ic p og ess. We ou line h ee
cons aining human ac o s, “pi all o scien i ic discipline,” “ he
dilemma o classi ica ion,” and “o e ly op imis ic expec a ions,”
which will equi e mul idisciplina y esea ch app oaches o
be conque ed.
Pi all o scien i ic discipline, i.e., dogma ic concep o ma ion
in scien i ic discipline, may cons ain one’s op ions. Con en ional
li e science disciplines, such as plan physiology, e olu iona y
ecology o phy opa hology, ei he la gely igno e mic obes
(Holland and Polacco, 1994; Compan e al., 2016; Kauppinen
e al., 2016; Saikkonen e al., 2016; an O e beek and Saikkonen,
2016) o examine mic obe–plan in e ac ions om limi ed,
p e-de ined pe spec i es, and la gely build on he knowledge
and adi ions o hei own discipline. Such s ongly canalized
app oaches limi ou abili y o acknowledge he complexi y o
biological in e ac ions and di e en le els o egula ion and
selec ion (Koskella e al., 2017).
Fo example, phy opa hology examines pa hogen–hos plan
in e ac ions ocusing on he ecology and e olu ion o pa hogen–
hos in e ac ions, and how hese in e ac ions migh be modula ed
by mic obial communi y in e ac ions in he pa hobiome
(Vayssie -Taussa e al., 2014). Al hough communi y-le el
app oaches ha include o he mic obial plan associa es a e
inc easingly being adop ed in plan pa hology (San hanam e al.,
2015; Syed Ab Rahman e al., 2018), a signi ican p opo ion o
phy opa hology esea ch is dedica ed o epidemiology, disease
diagnosis, and managemen o mic obial species o economic o
en i onmen al impo ance alone. This, combined wi h he long
adi ion o one mic obe–one plan app oach in he ield, migh
o e emphasize he pa hogenic phase o he mic obe’s li ecycle
and di e a en ion om o he ele an aspec s o he same
mic obe–plan in e ac ion, and o e look he impac o whole
mic obiomes in disease de elopmen o ep ession.
Meanwhile, an inc easing numbe o e olu iona y ecology
s udies e eal ha he same mic obial species commonly occupy
se e al ecological niches. Thus, he na u e o mic obe–plan
in e ac ions is labile and con ex -dependen in ecological
and e olu iona y ime a he han always bene icial o
disad an ageous o he hos (Saikkonen e al., 1998, 2004;
Wäli e al., 2013; Rybako a e al., 2016; Selosse e al., 2018). The
same mic obial species migh be labeled a pa hogen, pa asi e, o
endophy e, and e e ed o by di e en names. Fo example, a
mu a ion o a single locus may con e a ungal plan pa hogen
o a non-pa hogenic endophy ic symbion (F eeman and
Rod iguez, 1993), and he na u e o he in e ac ion wi h he hos
plan is condi ioned on en i onmen al ac o s (e.g., he bi o y
o a ailable esou ces), li e-his o y cha ac e s, and gene ic
combina ions o he hos and he mic obe (Rybako a e al.,
2016). Likewise, he bac e ial species Cla ibac e michiganensis
is known as a plan pa hogenic species, and C. michiganensis
subspecies a e ega ded as qua an ine o ganisms. Howe e , an
endophy ic bac e ial s ain, Cla ibac e s En 12, isola ed om
subni al alpine plan s and classi ied as C. michiganensis, is shown
o inc ease he chilling ole ance o i s hos plan s, and has no
been epo ed o be pa hogenic (Ding e al., 2011; Eichenlaub
and Ga emann, 2011). Fu he , he e y same mic obial species
a e some imes named di e en ly in di e en con ex s. As o
he naming o mic obes, a common endophy e o bi ch ees,
Fusicladium be ulae, was named Ven u ia di icha by a o es
pa hologis . Ven u ia is a eleomo ph ( he sexual ep oduc i e
F on ie s in Ecology and E olu ion | www. on ie sin.o g 2Ma ch 2020 | Volume 8 | A icle 61
Saikkonen e al. Holis ic Phy obiome Resea ch
s age) and is now i s o mal name, bu he ac is he species is a
bio ophic pa hogen and is mo e commonly an asymp oma ic
anamo phic (an asexual ep oduc i e s age) endophy e han
ob iously pa hogenic (Ahlholm e al., 2002a;Helande e al.,
2007). Simila ly, some plan mu ualis ic myco hizal ungi
a e epo ed as asymp oma ic endophy es and o ganic ma e
deg ading sap o ophs (Weiß e al., 2016; G ele e al., 2017;
Smi h e al., 2017; Ma ino e al., 2018; Schneide -Maunou y
e al., 2018). The ques ion is whe he we should conside a
mic obe sap ophy ic o pa hogenic i i inhabi s i s hos plan
asymp oma ically h oughou mos o i s li e cycle—in he case
o pe ennial hos s, pe haps o e yea s—and mani es s i sel as
pa hogenic o sap ophy ic du ing only a sho pe iod o i s li e.
Simila ly o scien i ic disciplines, he dilemma o classi ica ion,
i.e., g ouping mic obes ei he based on hei axa o unc ional
ole, di ec s and limi s esea che s’ in e es s o di e en pa s
o mic obial communi ies. Consequen ly, he ela ed scien i ic
heo ies ha e la gely de eloped sepa a ely ( an O e beek and
Saikkonen, 2016). Fo example, bac e ia, ungi, and i uses
a e usually s udied sepa a ely, al hough hey coexis and likely
o en in e ac wi h each o he (Saikkonen e al., 2004; an
O e beek and Saikkonen, 2016). Fu he mo e, in ecological and
e olu iona y li e a u e mic obe–plan in e ac ions a e gene ally
ea ed sepa a ely om he species–species and mul i ophic
in e ac ions o highe o ganisms (e.g., plan –he bi o e
in e ac ions), al hough all plan and animal in e ac ions
una oidably in ol e mic obes. We belie e ha unde s anding
any biological in e ac ion equi es aking mic obiomes o highe
o ganisms in o accoun , because oge he he o ganism and he
di e se assemblages o i s symbio ic mic obes o m a holobion ,
an ex ended pheno ype and he a ge o pheno ypic selec ion.
This concep o holobion should include all plan associa ed
mic obes whene e expe imen ally easible.
Finally, o e ly op imis ic expec a ions commonly eme ge
when a scien is assembles in o ma ion, becomes exci ed
by a ac i e disco e ies, concep s and/o economically
p o i able applica ion oppo uni ies, and po en ially misses
undamen al biological backg ound knowledge. Me agenomic
and p o eomic app oaches illumina e he ubiqui y, di e si y,
and impo ance o mic obes, and open ou eyes o associa ed
po en ial oppo uni ies. E idence shows ha he majo i y
o mic oo ganisms de ec ed by me agenomic ools colonize
hei hos plan s asymp oma ically (Compan e al., 2016;
Gopal and Gup a, 2016; Nissinen e al., 2019). These mic obial
associa es o plan s a e commonly de ined as endophy es
(Wilson, 1995). Taxonomically, endophy es a e di e se; hey
include a chaeal, bac e ial, ungal, and p o is ic mic oo ganisms.
Mos a e conside ed plan commensals bu ew, such as he
ungal Epichloë species commonly inhabi ing cool-season
g asses, a e ega ded as mu ualis ic, especially in high-nu ien
ag oecosys ems (Kauppinen e al., 2016; Saikkonen e al., 2016).
Plan mu ualis ic bac e ial endophy es a e less documen ed,
bu accumula ing genomic and me abolomic in o ma ion on
bac e ial genomes and modula ions in plan me abolism s ongly
sugges s hey ha e a ole in plan g ow h, de elopmen , and
s ess ole ance (Sessi sch e al., 2012; Ha doim e al., 2015;
an O e beek and Saikkonen, 2016; Esmaeel e al., 2018).
Inspi ed by e idence ha endophy ic mic oo ganisms a e
in ol ed in deni i ica ion, ni ogen ixa ion, and g eenhouse
gas emissions, and ha hey can a ec plan ole ance o
abio ic s ess, and i ually all ypes o plan –plan , plan –
he bi o e o plan –pa hogen in e ac ions, an inc easing
numbe o scien is s ha e become in e es ed in he po en ial
o endophy ic mic oo ganisms in he bioeconomy. He e
we p opose ha his de elopmen migh ha e di ec ed he
ocus on o e ly ambi ious goals and expec a ions o he
ollowing easons.
The mo e we look a he basic biology o mic obes, he
mo e ob ious i becomes ha al hough we could go e n
endophy ic mic obes, we canno ully con ol hem, especially
in he ag icul u al ields and na u e. Mic obial in e ac ions
a e known o be labile and con ex dependen anging om
an agonis ic o mu ualis ic in bo h ecological and e olu iona y
ime (Saikkonen e al., 1998, 2004; Lopes e al., 2009; Be g
e al., 2016; B ade e al., 2017). Mic obes ha e po en ial o
e ol e apidly as esponse o changing selec ion o ces, and
he eby a ec na u e o hei in e ac ion wi h he hos as well
as associa ed communi y and ecosys em p ocesses (F eeman and
Rod iguez, 1993; Saikkonen e al., 2004; e Ho s e al., 2014).
Thus, mu ualis ic, commensalis ic and an agonis ic mic obial
axa a e insepa able and p esen in i ually all mic obiomes
s udied. We should aim o unde s and he mic obiome dynamics,
and conside mic obes as pa o he di e se mul i-kingdom
communi y ( an Elsas e al., 2012; Koch e al., 2018), pa icula ly
when u ilizing plan mu ualis ic endophy es in sus ainable
ag icul u e and ood p oduc ion.
FUTURE PERSPECTIVES
Recen plan mic obiome esea ch is la gely ocused on
desc ibing s uc u e and unc ions o mic obial communi ies in
di e en plan associa ed niches, and linking speci ic mic obial
axa o plan pe o mance. Una guably, hese s udies ha e
apidly gi en us solid unde s anding o b oad axonomic ends
in plan associa ed mic obio a. In eg a ion o me agenomics
o p o eomics, me abolomics and o he omics-app oaches is
now enabling associa ing mic obiome s uc u al shi s o plan
holobion unc ioning. Howe e , he mass o da a p o ided
by hese echniques can easily o e whelm esea che s ha
cu en ly o en lack he ools o o ganize and p ocess he da a,
esul ing in low o pape s ca aloging plan and/o mic obial
unc ions o e en unanno a ed genes. He e, in eg a ion o
ecological heo ies in hese s udies (as also esea che aining)
would p o ide s uc u ing amewo k, connec ing now la gely
sepa a ed mic obiome esea ch o o he ields o plan -mic obe
in e ac ions and ecological and e olu iona y biology.
Indeed, plan mic obiome esea ch is ansi ioning om
desc ip i e su eys o comp ehensi e unde s anding o he plan
holobiome in he eco-e olu iona y amewo k. Iden i ica ion
o keys one mic obial species and in e connec ed mic obial
hubs, as well as hei pu a i e unc ions (Sessi sch e al., 2012;
Agle e al., 2016; Saikkonen e al., 2016; an de Heijden
and Ha mann, 2016), a e he basic pieces equi ed o sol e
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Saikkonen e al. Holis ic Phy obiome Resea ch
he eco-e olu iona y puzzle, comp ised o in e ac ing ee-li ing
mic obes and holobiome-uni s in ecosys ems.
Easy da a acquisi ion has c ea ed he illusion o con ollabili y
and he hope o mic obiology-based inno a ions. This has led o
he enaissance o mic obial esea ch seeking solu ions o global
issues such as diseases, ood secu i y, and sus ainable ag icul u al
p ac ices (Duhamel and Vandenkoo nhuyse, 2013; Kauppinen
e al., 2016; Busby e al., 2017; Finkel e al., 2017). Howe e , he
majo challenge is ha we a e s ill a long way om unde s anding
mic obial e sa ili y and how i ela es o he ecology and
e olu ion o plan holobion s in e ac ing wi h each o he and
hei en i onmen . Mee ing hese challenges equi es combining
no el molecula and mic obiological ools wi h empi ical and
heo e ical biological app oaches including ecology, gene ics and
epigene ics, pheno ypic e olu ion, and coe olu ion o in e ac ing
species. O he wise we lack heo e ical insigh s (P osse e al.,
2007), and igno e he complexi y and dynamics o mic obe–plan
in e ac ions in man-made and na u al ecosys ems.
We p opose ha o assemble he plan holobiome puzzle,
u u e wo k should ake in o accoun he ollowing p emises
and p esump ions.
Fi s , he majo i y o plan -mic obe s udies a e ei he plan
o mic obe cen e ed. Acco dingly, s udies a e o en designed
and in e p e ed wi h ei he he plan as he ac i e membe
which ec ui s i s mic obes (Geh ing and Whi ham, 1994) o
he hos plan as a backg ound a iable (e.g., “plan geno ype”)
o a habi a . Ins ead, bo h he plan and associa ed mic obes
should be aken in o accoun as ac i e membe s o he in e ac ion
(Saikkonen e al., 1999; Bulga elli e al., 2012; Dini-And eo e
and Raaijmake s, 2018). This equi es de eloping ue dialogue,
ecip ocal unde s anding, and mu ual collabo a ion be ween
esea che s om di e en li e science ields.
Second, we con end ha mic obe–plan in e ac ions ollow
simila e olu iona y and ecological p ocesses as hos –pa hogen
o hos –pa asi e in e ac ions, and he e o e need no o be
ea ed di e en ly (Saikkonen e al., 2004; Co do ez e al., 2019).
The p e ailing insigh is ha like o he species in e ac ions,
e en obliga e mic obe-plan mu ualism is based on mu ual
exploi a ion a he han ecip ocal al uism and bene i s o
he pa ne s a e only a ely symme ic (Thompson, 1994;
Mayna d Smi h and Sza hma y, 1995; Doebeli and Knowl on,
1998; Saikkonen e al., 2004). Symbioses be ween mic obes
and hei hos plan s may also in ol e ecip ocal manipula ion
o pheno ypes, including mo phology and physiology, and
li ecycle o pa ne s (Saikkonen e al., 2016). Thus, con lic ing
selec ion o ces a e likely o des abilize hem, and he ou come
o in e ac ions can change in ime and space p ojec ing he
ecological su ace o a dynamic i ness landscape wi h adap i e
peaks and alleys (Thompson, 1994, 2005; Saikkonen e al.,
2004). Fo example, mu ualis ic myco hizae and Epichloë
endophy es can become pa asi ic in he p esence o he bi o es o
hemipa asi ic plan s especially in esou ce-limi ed en i onmen s
(Ahlholm e al., 2002b; Leh onen e al., 2005; Saikkonen e al.,
2010a; Wäli e al., 2013).
Thi d, co-occu ing plan -associa ed mic obes, i espec i e o
axa, a e likely o in e ac wi h each o he . Mic obes compe e,
in e ac chemically, and/o media e he hos quali y o each o he .
Chemical in e play may include signaling and chemical c oss-
alk among mic obes and hei hos plan cells (Hamil on e al.,
2012; Compan e al., 2016; an O e beek and Saikkonen, 2016)
bu can also ex end o co e o he o ganisms eeding on he
sha ed hos plan as well as associa ed ood webs (Leh onen
e al., 2006; Saikkonen e al., 2006; Saa i e al., 2010; Li e al.,
2014). I is no ewo hy ha ce ain pa hways egula ing plan
esponses o he e o ophic o ganisms, such as salicylic acid and
jasmonic acid pa hways, ha e been shown o coun e ac (Balla é,
2011; Thale e al., 2012; Pineda e al., 2013). Fo ins ance,
chemical c oss alk be ween mu ualis ic mic obes, bio ophic and
nec o ophic pa hogens (Bas ias e al., 2018), and he bi o es
may cons ain he hos plan om eaching op imal pa hogen-
o he bi o e-speci ic esis ance (Ahlholm e al., 2002a), bu is
likely o be bene icial o o e all i ness o he holobion . Simila ly,
communi y-le el app oaches o bac e ial and ungal in e ac ions
a e needed o unde s and he impo ance o he s uc u e and
unc ions o mic obial communi y associa ed wi h plan s on
plan pe o mance as well as on ecosys em unc ions and se ices
(Dini-And eo e and Raaijmake s, 2018). Mo e knowledge abou
mul ispecies coe olu ion is necessa y o ully unde s and any
pa icula bipa i e mic obe–plan in e ac ions and how hey
modula e cascading in e ac ions ac oss ophic laye s.
Fou h, he pe o mance o plan -associa ed o ganisms such
as mu ualis ic, commensalis ic, and an agonis ic mic obes, as
well as he bi o es, may also be a esponse o gene ically o
epigene ically de e mined plan ai s a he han in e connec ed
associa ions among hem. The ole o epigene ics is s ill poo ly
unde s ood. In con as , empi ical e idence sugges s ha o
example gene ic compa ibili y can de e mine endophy ic
mic obe-plan combina ions ha can be mu ualis ic o
commensalis ic depending on en i onmen al condi ions
(Saikkonen e al., 2010b). Fu he mo e gene ically de e mined
plan ai s can de e mine plan quali y o he e o ophic
o ganisms such as mic obes and/o he bi o es (F i z and Simms,
1992) and gene ic co ela ions be ween plan esis ance o
pa hogens and he bi o es ha e been sugges ed o cons ain
plan s om eaching op imal species-speci ic esis ance
(Ahlholm e al., 2002a).
Fi h, mic obes a e highly di e se and e sa ile, and he
ecological ole o mic obes is o en complex and liable o
change. Mic obes can occupy se e al ecological niches ha
may o e lap, and he na u e o mic obe–plan associa ion
is con ex dependen . The same ecological unc ion can be
p o ided by se e al di e en mic obes, and indi idual mic obes
can be—a leas pa ially—subs i u able by o he s. This calls
impo ance o s udies on he mic obial media ed key unc ions
in di e en en i onmen s.
The spec um, complexi y, and dynamics o mic obe–plan
in e ac ions demons a e ha plan mic obiomes p o ide a
e ile g ound o unde s anding uni o selec ion, mul i ophic
in e ac ions, e olu ion o li e his o ies, and co-e olu iona y
p ocesses, and how mic obiomes should be aken in o accoun
when de eloping mic obe-based bio echnologies and ecosys em
se ices. Two unanswe ed ques ions emain: (1) How plan s
and hei associa ed mic obes indi idually and/o in conce
as a pheno ypic uni espond o p e ailing selec ion p essu es?
F on ie s in Ecology and E olu ion | www. on ie sin.o g 4Ma ch 2020 | Volume 8 | A icle 61

Saikkonen e al. Holis ic Phy obiome Resea ch
(2) Wha p opo ion o ecological ou come is de e mined by
gene ics, epigene ics, and pheno ypic plas ici y in he ecologically
ele an ai s, and hus in he adap i e adia ion o holobion s?
P esen ba ie s mus be disman led in o de o dissemina e
cu en knowledge o plan mic obiomes and c ea e a mo e
concep ual amewo k wi h empi ical and heo e ical examples,
and p edic able hypo heses ( an O e beek and Saikkonen, 2016;
F ank e al., 2017).
This knowledge is u gen ly needed o ackle he o emos
global challenges o ou imes: he biodi e si y loss, clima e
change and he inc easing demand o ood p oduc ion o
mee wo ld’s popula ion g ow h (Sp ingmann e al., 2018;
Tolle son, 2019). Fo example, in he deba e on biodi e si y
loss and endange ed species, pa icula a en ion should be paid
o he impo ance o abundan keys one species main aining
c ucial ecosys em unc ions ha a e i al o h i ing ecosys ems
o species ha may h ea en o he species by dis up ing
ecosys em unc ions. Mic obes a e la gely igno ed in his
con ex al hough hey a e essen ial o p ocesses ha make
Ea h habi able o p ima y p oduce s and o he o ganisms
subsis ing on hem. Simila ly mic obes should be aken in o
accoun in isk analyses and solu ions o aim mi iga ing clima e
change as well as in sus ainable ood p oduc ion (Duhamel
and Vandenkoo nhuyse, 2013; Gundel e al., 2013; Kauppinen
e al., 2016). Fo example, ecen e idence sugges s ha
mic obes can inc ease ca bon sink in e es ial ecosys ems by
enhancing ca bon up ake in o soils and in o plan s by p omo ing
plan g ow h (e.g., myco hizae, hizobia and endophy es)
o al e he lux o g eenhouse gases om he soil o he
a mosphe e (Clemmensen e al., 2013; Iqbal e al., 2013;
A e ill e al., 2014). Bene icial mic obial plan symbion s
ha e been sugges ed o ha e g ea po en ial in sus ainable
ag icul u al and ho icul u al p ac ices, and o en i onmen al
imp o emen as well (Duhamel and Vandenkoo nhuyse, 2013;
Gundel e al., 2013; Kauppinen e al., 2016). These goals
migh pa ly be o e ly ambi ious because mic obe-plan
in e ac ions a e complex, labile and con ex dependen , and
hus, we ne e can ully con ol plan associa ed mic obiomes
in na u e. Howe e , some o hese ambi ious goals can be
a ained i we in es esou ces in mul idisciplina y collabo a ion
ac oss a ious ields o expe ise, as unde s anding he plan -
mic obiome dynamics and ac o s impac ing holobion ecology
and e olu ion can enable us o u ilize he plan mic obiomes o
sus ainable u u e.
AUTHOR CONTRIBUTIONS
KS, RN, and MH ha e con ibu ed equally in ini ializing,
inno a ing, and w i ing he pape .
FUNDING
This wo k was suppo ed by he Academy o Finland, G an Nos.
295976 and 326226 and Finnish Cul u al Founda ion.
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F on ie s in Ecology and E olu ion | www. on ie sin.o g 7Ma ch 2020 | Volume 8 | A icle 61