Recei ed: 16 Augus 2023 Re ised: 17 Sep embe 2023 Accep ed: 4 Oc obe 2023
DOI: 10.1002/bies.202300153
COMMENTARY
Though s & Opinion
A case o he impo ance o ollowing an ibio ic esis an
bac e ia h oughou he soil ood web
Ca los Ga bisu1I zia Alko a2
1NEIKER −Basque Ins i u e o Ag icul u al
Resea ch and De elopmen , De io, Spain
2Depa men o Biochemis y and Molecula
Biology, Uni e si y o he Basque Coun y
(UPV/EHU), Bilbao, Spain
Co espondence
I zia Alko a, Depa men o Biochemis y
and Molecula Biology, Uni e si y o he
Basque Coun y (UPV/EHU), P.O. Box 644,
48080 Bilbao, Spain.
Email: i zi.alk[email p o ec ed]
Funding in o ma ion
MCIN/AEI/10.13039/501100011033,
G an /Awa d Numbe :
PID2020-116495RB-I00; Basque
Go e nmen , G an /Awa d Numbe :
IT1578-22; JRL En i onmen al An ibio ic
Resis ance
Abs ac
I is necessa y o complemen nex -gene a ion sequencing da a on he soil esis ome
wi h heo e ical knowledge p o ided by ecological s udies ega ding he sp ead o
an ibio ic esis an bac e ia (ARB) in he abio ic and, especially, bio ic ac ion o he
soil ecosys em. Pa icula ly, when ARB en e ag icul u al soils as a consequence o he
applica ion o animal manu e as e ilize , om a mic obial ecology pe spec i e, i is
impo an o know hei a e along he soil ood web, ha is, h oughou ha complex
ne wo k o eeding in e ac ions among membe s o he soil bio a ha has c ucial
e ec s on species ichness and ecosys em p oduc i i y and s abili y. I is c i ical o
s udy how he ARB ha en e he soil h ough he applica ion o manu e can each
o he axonomical g oups (e.g., ungi, p o is s, nema odes, a h opods, ea hwo ms),
paying special a en ion o hei p esence in he gu mic obiomes o meso auna-
mac o auna and o he possibili ies o ho izon al gene ans e o an ibio ic esis an
genes.
KEYWORDS
An ibio ic esis ance, gu mic obiomes, ho izon al gene ans e , manu e, mic obial ecology,
o ganic a ming, soil bio a
COMMENTARY
An ibio ic esis ance is a global heal h p oblem o he u mos impo -
ance. The s udy o he eme gence, dissemina ion, and e olu ion o
an ibio ic esis an bac e ia (ARB), ha bou ing an ibio ic esis ance
genes (ARGs), is o en claimed o equi e a One Heal h app oach.
Then, in he las decades, much esea ch has been done on he links
be ween he human esis ome and he en i onmen al esis ome ( he
esis ome is he collec ion o all he ARGs and hei p ecu so s p esen
in pa hogenic and non-pa hogenic bac e ia). I is impo an o empha-
size ha mic oo ganisms (e.g., bac e ia, ungi) ha e used an ibio ics, o
compe i ion pu poses o as signalling molecules ha acili a e in a- o
in e species in e ac ions wi hin mic obial communi ies,[1] o millions
o yea s. The e o e, ARB and ARGs a e o en isola ed om p is ine
en i onmen s, no subjec ed o an ibio ic esidues de i ed om human
This is an open access a icle unde he e ms o he C ea i e Commons A ibu ion-NonComme cial-NoDe i s License, which pe mi s use and dis ibu ion in any
medium, p o ided he o iginal wo k is p ope ly ci ed, he use is non-comme cial and no modi ica ions o adap a ions a e made.
© 2023 The Au ho s. BioEssays published by Wiley Pe iodicals LLC.
usage, indica ing ha he esis ome is an in eg al pa o he mic obial
ecology o he di e en en i onmen al compa men s.
Due o he use o an ibio ics in li es ock, he e a e many s udies on
he po en ial consequences o e iliza ion wi h animal manu e o he
in oduc ion o ARB and ARGs, he la e in many cases associa ed wi h
mobile gene ic elemen s (MGEs), in ag icul u al soils, wi h concomi an
isks o human heal h ia he consump ion o c ops, especially esh
ho icul u al p oduce.
In app oxima ely he pas decade, as a esul o he ema kable
de elopmen o ad anced sequencing echnologies and bioin o ma ics
ools, mos o hese s udies on he impac o e iliza ion wi h animal
manu e on he soil esis ome ( he esis ance de e minan s p esen in
he soil) ha e been ocused on he use o nex -gene a ion sequencing
(NGS), pa icula ly 16S RNA amplicon sequencing and me agenomics
( ia, e.g., sho gun sequencing wi h Illumina, Ox o d nanopo e o PacBio
BioEssays. 2023;45:2300153. wileyonlinelib a y.com/jou nal/bies 1o 4
h ps://doi.o g/10.1002/bies.202300153
GARBISU and ALKORTA 2o 4
echnologies), o de e mine he p esence and abundance o ARGs
and MGE- ela ed genes in soils, as well as hei po en ial ela ion-
ship wi h bac e ial axonomic g oups (i.e., o es ablish possible links
be ween unc ional and s uc u al- axonomic-phylogene ic in o ma-
ion). Fo he de ec ion and quan i ica ion o hese unc ional genes,
high- h oughpu qPCR has also been used ex ensi ely.
Al hough he e is no doub ha molecula echnologies and NGS in
pa icula ha e b ough g ea p og ess and no el insigh s o he soil
mic obial ecology ield (mos o all, he disco e y o he ex emely high
ichness o soil mic obial communi ies), p ima ily hanks o he pos-
sibili y o o e coming he limi a ions o cul i a ion-based echniques,
la ely, i is o en poin ed ou ha , because o he cu en gene-cen ic
app oach, many o he ecen soil mic obial ecology s udies (e.g., soil
esis ome s udies) a e o a desc ip i e, co ela ion-based, and/o
pa e n-seeking na u e, and ha e seldom con ibu ed o signi ican
ad ances in knowledge and unde s anding o he ecology o soil
mic oo ganisms, no ha e subs an ially inc eased ou capaci y o p e-
dic soil mic obial communi y composi ion, dynamics, and esilience,
no un a elled he consequences o communi y composi ion o
soil p ocess a es and ecosys em unc ioning.[2]Then, he ield o
soil mic obial ecology in gene al, and he opic o he impac o he
applica ion o animal manu e on he soil esis ome in pa icula , need
o add ess key ecological ques ions and pe o m hypo hesis-based,
mechanism-based s udies ha con ibu e o he ad ance o mic obial
ecology heo y and applica ions.
Al hough, by de ini ion, he mic obial “ecology” ield mus inco po-
a e an ecological and ecocen ic app oach, in o de o a ac a en ion
o a gi en ield o knowledge, i is o en e y use ul o poin ou i s
po en ial links wi h human heal h and/o well-being om an an h o-
pocen ic poin o iew. In his espec , gi en he magni ude and
ele ance o he an ibio ic esis ance c isis, wi hou doub i can be
s a ed ha he soil esis ome and i s po en ial links wi h he human
esis ome is one o he soil opics o mo e in e es om an an h o-
pocen ic pe spec i e. A e all, an ibio ics, an ibio ic esidues ha
emain bioac i e, ARB, and ARGs a e no only en i onmen al eme ging
con aminan s o abio ic and bio ic na u e, espec i ely, bu a e pu ing
a isk one o he mos impo an co ne s one o mode n medicine, ha
is, an ibio ics.
On he o he hand, he ood web ( he complex ne wo k o in e con-
nec ing and o e lapping ood chains in an ecosys em) is a key ecological
concep o pa amoun impo ance o he unde s anding o ecosys em
unc ioning. Food webs ep esen complex ecological ne wo ks whose
opologies ha e been widely used in ecology o illus a e he s uc u al
and unc ional p ope ies o biological communi ies and ecosys ems.
Explici ly, ood webs a e ep esen a ions o species and hei eed-
ing ela ionships. The nodes a e o en e med “ ophic le el species o
ophospecies” and he links ha e lec he di ec ion o in e ac ions
“ ophic in e ac ions” (e.g., who is he p ey and who is he p eda o ).
Al hough a discussion on he as complexi y o he soil ood webs
and he ongoing deba es on hei s uc u e and opology is no wi hin
he scope o his commen a y ( o a highly simpli ied ep esen a ion
o he soil ood web, see Figu e 1), om he pi o al wo k o Hun
and colleagues,[3] hey a e o en ep esen ed as webs compa men-
alised in o bac e ial-based and ungal-based ene gy channels (wi h
some webs domina ed by bac e ia and o he s by ungi) uni ed a highe
ophic le els occupied by p o is s-p o ozoa, nema odes, a h opods,
ea hwo ms, insec s, small e eb a es, and so o h.
When ARB ha bou ing ARGs en e he soil ecosys em du ing he
applica ion o animal manu e as e ilize (an ag icul u al p ac ice
being encou aged, due o i s many p o en bene i s, unde a a ie y
o ag icul u al sys ems such as o ganic a ming, egene a i e ag icul-
u e, ecological ag icul u e, and ag oecology), hey can be iewed as
“in asi e species” whose ecological success will depend on a a ie y
o abio ic and bio ic ac o s (e.g., hei ecological alence unde he
speci ic soil physicochemical condi ions, hei ecological i ness and
compe i i eness, hei capaci y o acclima ion and adap a ion, hei
dispe sal abili ies, and so on). In his espec , in a s udy on he ba -
ie s ha mic obial di e si y can p o ide agains mic obial in asion
by ARB, soil mic obial di e si y was ound o be nega i ely co ela ed
wi h he abundance o ARGs and, hen, he au ho s concluded ha a
high mic obial di e si y in soil can ac as a biological ba ie agains
he sp ead o an ibio ic esis ance.[4]Likewise, clinical class 1 in e-
g ons, MGEs ha ha e been widely ecognized as majo con ibu o s
o he e olu ion and dissemina ion o an ibio ic esis ance, ha e been
epo ed as in asi e species[5]wi h a decisi e ole in he an ibio ic
esis ance c isis. These in eg ons ha e in aded many bac e ial axa,
hei hos s, and, c i ically, all en i onmen s associa ed wi h human
ac i i y.[5]
Ano he use ul concep ual app oach o he in es iga ion o he
in oduc ion o ARB in soil ia animal manu e is he s udy o commu-
ni y coalescence ( he mixing o di e en biological communi ies),[6]a
p ocess wi h many ami ica ions o communi y s uc u e and unc ion,
shaped, among many o he ac o s, by he ypes o in e ac ions and
by a ious p ocesses o communi y assembly such as selec ion, d i ,
dispe sal, and di e si ica ion.
When en e ing ag icul u al soil, among o he possibili ies, he ARB
ini ially p esen in he manu e can (i) die owing o, o ins ance, lack o
adap a ion o he new en i onmen al condi ions, poo ecological com-
pe i i eness, p eda ion, and so o h; (ii) su i e and hen inhabi he
inanima e componen o he soil ma ix, li ing as ee li ing cells in he
soil po es o , mo e o en, wi hin bio ilms a ached o he soil agg e-
ga es, in ac i e o do man o ms; and (iii) su i e a e being inges ed
by, o associa ed wi h, membe s o o he axonomical g oups o he soil
ood web; in his espec , in many cases, hey end up inhabi ing he gu
mic obiome o species belonging o he soil meso auna o mac o auna.
F om all o he abo e, in his commen a y a icle, we p opose ha ,
ega ding he soil esis ome, i is c i ical o complemen he my iad o
gene-cen ic NGS s udies wi h ecology-cen ed s udies. In pa icula ,
among hese ecology-cen ed s udies, we p opose ha hose deal-
ing wi h he dissemina ion o he ARB ini ially p esen in he animal
manu e used o ag icul u al e iliza ion should ideally ollow o e
ime all possible biological-ecological ou es o p opaga ion h ough-
ou he soil ood web, by means o ARB iden i ica ion and s udy in soil
ungi, p o ozoa, nema odes, a h opods, ea hwo ms, insec s and so
o h. O cou se, his p oposal does no exclude he s udy and moni-
o ing o he a e o hose same ARB in he soil ma ix i sel , ega ding
hei ans o ma ion in o bac e ia ha will li e in he po es and, mo e
o en, wi hin bio ilms a ached o soil agg ega es.
15211878, 2023, 12, Downloaded om h ps://onlinelib a y.wiley.com/doi/10.1002/bies.202300153 by Uni e sidad Del Pais Vasco, Wiley Online Lib a y on [26/12/2023]. See he Te ms and Condi ions (h ps://onlinelib a y.wiley.com/ e ms-and-condi ions) on Wiley Online Lib a y o ules o use; OA a icles a e go e ned by he applicable C ea i e Commons License
3o 4 GARBISU and ALKORTA
FIGURE 1 Simpli ied ep esen a ion o he soil ood web. The biomass o each le el dec eases because a conside able amoun o ene gy is los
(e.g., dissipa ed as hea ) wi h each ans e as en opy inc eases. I is p oposed o ollow an ibio ic esis ance bac e ia h oughou he soil ood web.
Fu he mo e, we p opose o pay special a en ion o (i) he possibil-
i y o ho izon al gene ans e (HGT) among he di e en axonomical
g oups o he soil ood web, as his phenomenon o la e al gene ans e
does no only occu among bac e ia o be ween bac e ia and a chaea,
bu also be ween p oka yo es and euka yo es; and (ii) he p esence o
ARB in he gu mic obiomes o he soil meso auna and mac o auna.
Fo example, HGT s udies can be pe o med in i o, using a ailable
cul i a ion-dependen classical and/o high- h oughpu conjuga ion
assays, wi h he isola ed en i onmen al ARB as dono and ecipien
bac e ia (en i onmen al pe spec i e), o al e na i ely wi h he isola ed
ARB as dono s and po en ial human pa hogens (e.g., Esche ichia coli)as
ecipien s (an h opocen ic pe spec i e).
Unlike many s udies ha a e ocused on he p esence o ARB and,
abo e all, ARGs in he gu mic obiomes o speci ic axa o he soil meso-
auna o mac o auna a a gi en poin in ime, we p opose o s udy o e
ime he p opaga ion o ARB in all o , ailing ha , in as many as possi-
ble axa o he soil ood web in he same soil, in an a emp o achie e
a comp ehensi e, empo al, and dynamic ep esen a ion o he di e -
en soil biological-ecological ou es ha ARB can ollow once hey ha e
been in oduced in o ag icul u al soil.
We a e ce ainly awa e o he ac ha his p oposal can p o e
a somewha daun ing ask bu , a he same ime, we do eckon ha
his ecological-ecocen ic app oach, as compa ed o he gene-cen ic
app oach, has he po en ial o gene a e much needed mic obial ecol-
ogy knowledge, as well as o b ing ou impo an scien i ic ques ions
and hypo heses o he soil mic obial ecology ield in ela ion o (i) he
links be ween he soil esis ome and he human esis ome, a opic o
much alue and in e es om a One Heal h pe spec i e; and (ii) he su -
i al and ecological implica ions o he in oduc ion and p opaga ion o
ARB in ag icul u al soils, a subjec o much ele ance o he biodi e -
si y, unc ioning, esis ance, and esilience o he soil ecosys em, whose
heal h is c i ical o he p o ision o essen ial se ices and, in gene al, o
he unc ioning o e es ial ecosys ems.
On he posi i e side, i mus be s a ed ha new de elop-
men s in molecula p obes, luo escen p obes, low cy ome y,
ad anced mic oscopy (e.g., Raman mic o-spec oscopy, FT-IR mic o-
spec oscopy), and o he analy ical echniques a e acili a ing he
acking and moni o ing o bac e ia in soil. On he nega i e side, i mus
be men ioned ha soil ood webs a e ex emely complex, o en wi h
i e ophic le els, and no well unde s ood. P eda o s in soil ood webs
appea o be gene alis s (e en wi h omni o ous eeding habi s), hus
being able o inges o ganisms om a ious ophic le els, which means
ha hey can acqui e bac e ia om o ganisms belonging o di e en
ophic le els.
Finally, a ew s udies ela ed o he opic unde conside a ion he e
a e b ie ly p esen ed. Since bac e ia and ungi a e he dominan g oups
o soil bio a in e ms o bo h abundance and di e si y, i is no su -
p ising ha hey cons an ly in e ac , physically and me abolically, wi h
each o he . Fungal hyphae p o ide a habi a o bac e ial communi-
ies ha can o m bio ilms on hem (he e, i mus be emembe ed
ha wi hin bio ilms, he HGT o ARGs is o en in ensi ied), bu , mos
impo an ly, ungal hyphae se e as ec o s o bac e ia (e.g., ARB)
o a el ac oss he soil, he so-called hyphal highways along which
bac e ia can swim in he wa e ilm ha coa s he hyphae. Al e na-
i ely, bac e ia can a el passi ely by se ling a he ip o he g owing
hyphae.[7]
15211878, 2023, 12, Downloaded om h ps://onlinelib a y.wiley.com/doi/10.1002/bies.202300153 by Uni e sidad Del Pais Vasco, Wiley Online Lib a y on [26/12/2023]. See he Te ms and Condi ions (h ps://onlinelib a y.wiley.com/ e ms-and-condi ions) on Wiley Online Lib a y o ules o use; OA a icles a e go e ned by he applicable C ea i e Commons License
GARBISU and ALKORTA 4o 4
Pe aining o p o is s, al hough soil p o ozoa a e known o eed
on bac e ia, many bac e ia engul ed in he esicles o p o ozoa ha e
he capaci y o a oid being diges ed, hus opening up oppo uni ies
o cell- o-cell con ac among bac e ia p esen in he esicles, esul -
ing, o ins ance, in some p o ozoa enhancing he equency o ARG
conjuga ion among hem.[8]
Mo eo e , ARGs ha e been ound o be di e se and abundan in
nema ode gu mic obiomes and, mos impo an ly, o ha e he capaci y
o be ans e ed along belowg ound ood chains.[9]
In ela ion o a h opods, i has been epo ed ha an ibio ic expo-
su e can al e he gu mic obiome o he common soil collembolan
Folsomia candida and signi ican ly inc ease he di e si y and abundance
o ARGs in he collembolan gu .[10]
In e es ingly, an ibio ic-p oducing S ep omyces (a genus o soil ac i-
nobac e ia well-known o hei capaci y o p oduce an ibio ics and
o he seconda y me aboli es used in human medicine) and o he ac i-
nobac e ia can li e as symbion s o soil in e eb a es, whe e hey play
a p o ec i e ole by p oducing an ibio ics ha a e used o de end he
hos s agains bac e ial in ec ions.[11]These symbioses in which he
hos eeds and p o ec s he ac inobac e ia and, in e u n, he ac i-
nobac e ia p oduce an ibio ics o p o ec he hos om pa hogens a e
mos in e es ing o he s udy o he sp ead and e olu ion o ARB, as
S ep omyces cells ca y esis ance o hei own an ibio ics and, unde
selec i e p essu e, hei ARGs can sp ead o o he bac e ia ia HGT.[11]
Al hough he ole o ea hwo ms in he sp ead o an ibio ic esis-
ance is s ill con o e sial, di e en s udies ha e shown ha manu e
e iliza ion can inc ease he abundance o ARGs in ea hwo m gu
mic obiomes,[12]a ac which mus in e p e ed aking in o close con-
side a ion he ole o ea hwo ms as ecosys em enginee s ha can
in luence he mo emen o o he soil o ganisms, including bac e ia.
To inish, we do hope his commen a y p omo es he de elopmen
o mo e ecologically ele an s udies on soil mic obial ecology and, in
pa icula on he opic o an ibio ic esis ance in soil.
AUTHOR CONTRIBUTIONS
I zia Alko a: Concep ualiza ion, w i ing – o iginal d a , w i ing –
e iew and edi ing; Ca los Ga bisu: Concep ualiza ion, w i ing – o ig-
inal d a , w i ing – e iew and edi ing.
ACKNOWLEDGEMENTS
This wo k was suppo ed by MCIN/AEI/10.13039/501100011033
(PID2020-116495RB-I00), Basque Go e nmen (IT1578-22), and
Euskampus – JRL En i onmen al An ibio ic Resis ance.
CONFLICT OF INTEREST STATEMENT
The au ho s decla e no con lic o in e es .
DATA AVAILABILITY STATEMENT
Da a sha ing is no applicable o his a icle as no da ase s we e
gene a ed o analysed du ing he cu en s udy.
ORCID
Ca los Ga bisu h ps://o cid.o g/0000-0002-5577-6151
I zia Alko a h ps://o cid.o g/0000-0001-6978-389X
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