Abstract
The general interest in microbial ecology has skyrocketed over the past decade, driven by technical advances and by the rapidly increasing appreciation of the fundamental services that these ecosystems provide. In biotechnology, ecosystems have many more functionalities than single species, and, if properly understood and harnessed, will be able to deliver better outcomes for almost all imaginable applications. However, the complexity of microbial ecosystems and of the interactions between species has limited their applicability. In research, next generation sequencing allows accurate mapping of the microbiomes that characterise ecosystems of biotechnological and/or medical relevance. But the gap between mapping and understanding, to be filled by “functional microbiomics”, requires the collection and integration of many different layers of complex data sets, from molecular multi-omics to spatial imaging technologies to online ecosystem monitoring tools. Holistically, studying the complexity of most microbial ecosystems, consisting of hundreds of species in specific spatial arrangements, is beyond our current technical capabilities, and simpler model systems with fewer species and reduced spatial complexity are required to establish the fundamental rules of ecosystem functioning. One such ecosystem, the ecosystem responsible for natural alcoholic fermentation, can provide an excellent tool to study evolutionarily relevant interactions between multiple species within a relatively easily controlled environment. This review will critically evaluate the approaches that are currently implemented to dissect the cellular and molecular networks that govern this ecosystem.
Key points
• Evolutionarily isolated fermentation ecosystem can be used as an ecological model.
• Experimental toolbox is gearing towards mechanistic understanding of this ecosystem.
• Integration of multidisciplinary datasets is key to predictive understanding.
Graphical abstract
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References
Albertin W, Chasseriaud L, Comte G, Panfili A, Delcamp A, Salin F, Marullo P, Bely M (2014) Winemaking and bioprocesses strongly shaped the genetic diversity of the ubiquitous yeast Torulaspora delbrueckii. PLoS One 9:e94246. https://doi.org/10.1371/journal.pone.0094246
Alonso A, de Celis M, Ruiz J, Vicente J, Navascués E, Acedo A, Ortiz-Álvarez R, Belda I, Santos A, Gómez-Flechoso MÁ, Marquina D (2019) Looking at the origin: some insights into the general and fermentative microbiota of vineyard soils. Fermentation 5:78. https://doi.org/10.3390/fermentation5030078
Andorrà I, Berradre M, Mas A, Esteve-Zarzoso B, Guillamón JM (2012) Effect of mixed culture fermentations on yeast populations and aroma profile. LWT - Food Sci Technol 49:8–13. https://doi.org/10.1016/j.lwt.2012.04.008
Bagheri B, Bauer FF, Cardinali G, Setati ME (2020) Ecological interactions are a primary driver of population dynamics in wine yeast microbiota during fermentation. Sci Rep 10:4911. https://doi.org/10.1038/s41598-020-61690-z
Bagheri B, Bauer FF, Setati ME (2017) The impact of Saccharomyces cerevisiae on a wine yeast consortium in natural and inoculated fermentations. Front Microbiol 8:1–13. https://doi.org/10.3389/fmicb.2017.01988
Bagheri B, Zambelli P, Vigentini I, Bauer FF, Setati ME (2018) Investigating the effect of selected non-Saccharomyces species on wine ecosystem function and major volatiles. Front Bioeng Biotechnol 6:1–12. https://doi.org/10.3389/fbioe.2018.00169
Baldini F, Heinken A, Heirendt L, Magnusdottir S, Fleming RMT, Thiele I (2019) The microbiome modeling toolbox: from microbial interactions to personalized microbial communities. Bioinformatics 35:2332–2334. https://doi.org/10.1093/bioinformatics/bty941
Bernasconi R, Stat M, Koenders A, Paparini A, Bunce M, Huggett MJ (2019) Establishment of coral-bacteria symbioses reveal changes in the core bacterial community with host ontogeny. Front Microbiol 10:1529. https://doi.org/10.3389/fmicb.2019.01529
Bernstein HC, Carlson RP (2012) Microbial consortia engineering for cellular factories: in vitro to in silico systems. Comput Struct Biotechnol J 3:e201210017. https://doi.org/10.5936/csbj.201210017
Bokulich NA, Collins TS, Masarweh C, Allen G, Heymann H, Ebeler SE, Mills DA (2016) Associations among wine grape microbiome, metabolome, and fermentation behavior suggest microbial contribution to regional wine characteristics. mBio 7:e00631. https://doi.org/10.1128/mBio.00631-16.Editor
Bokulich NA, Joseph CML, Allen G, Benson AK, Mills DA (2012) Next-generation sequencing reveals significant bacterial diversity of botrytized wine. PLoS One 7:e36357. https://doi.org/10.1371/journal.pone.0036357
Bokulich NA, Swadener M, Sakamoto K, Mills DA, Bisson LF (2015) Sulfur dioxide treatment alters wine microbial diversity and fermentation progression in a dose-dependent fashion. Am J Enol Vitic 66:73–79. https://doi.org/10.5344/ajev.2014.14096
Bokulich NA, Thorngate JH, Richardson PM, Mills DA (2014) Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc Natl Acad Sci 111:E139–E148. https://doi.org/10.1073/pnas.1317377110
Bordet F, Joran A, Klein G, Roullier-gall C, Alexandre H (2020) Yeast – yeast interactions: mechanisms, methodologies and impact on composition. Microorganisms 8:600. https://doi.org/10.3390/microorganisms8040600
Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ (2014) Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 7:339–362. https://doi.org/10.1201/b16586
Branco P, Kemsawasd V, Santos L, Diniz M, Caldeira J, Almeida MG, Arneborg N, Albergaria H (2017) Saccharomyces cerevisiae accumulates GAPDH-derived peptides on its cell surface that induce death of non-Saccharomyces yeasts by cell-to-cell contact. FEMS Microbiol Ecol 93:1–10. https://doi.org/10.1093/femsec/fix055
Brenner K, You L, Arnold FH (2008) Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol 26:483–489. https://doi.org/10.1016/j.tibtech.2008.05.004
Brown MR, Hands CL, Coello-Garcia T, Sani BS, Ott AIG, Smith SJ, Davenport RJ (2019) A flow cytometry method for bacterial quantification and biomass estimates in activated sludge. J Microbiol Methods 160:73–83. https://doi.org/10.1016/j.mimet.2019.03.022
Cani PD (2018) Human gut microbiome: hopes, threats and promises. Gut 67:1716–1725. https://doi.org/10.1136/gutjnl-2018-316723
Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA (2010) Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev 90:1103–1163. https://doi.org/10.1152/physrev.00038.2009
Ciani M, Beco L, Comitini F (2006) Fermentation behaviour and metabolic interactions of multistarter wine yeast fermentations. Int J Food Microbiol 108:239–245. https://doi.org/10.1016/j.ijfoodmicro.2005.11.012
Ciani M, Comitini F (2015) Yeast interactions in multi-starter wine fermentation. Curr Opin Food Sci 1:1–6. https://doi.org/10.1016/j.cofs.2014.07.001
Ciani M, Comitini F, Mannazzu I, Domizio P (2010) Controlled mixed culture fermentation: a new perspective on the use of non-Saccharomyces yeasts in winemaking. FEMS Yeast Res 10:123–133. https://doi.org/10.1111/j.1567-1364.2009.00579.x
Clark RT (2015) Imaging flow cytometry enhances particle detection sensitivity for extracellular vesicle analysis. Nat Methods 12:i–ii. https://doi.org/10.1038/nmeth.f.380
Comitini F, Gobbi M, Domizio P, Romani C, Lencioni L, Mannazzu I, Ciani M (2011) Selected non-Saccharomyces wine yeasts in controlled multistarter fermentations with Saccharomyces cerevisiae. Food Microbiol 28:873–882. https://doi.org/10.1016/j.fm.2010.12.001
Conacher CG, Naidoo-Blassoples RK, Rossouw D, Bauer FF (2020) Real-time monitoring of population dynamics and physical interactions in a synthetic yeast ecosystem by use of multicolour flow cytometry. Appl Microbiol Biotechnol. 12:5547–5562. https://doi.org/10.1007/s00253-020-10607-x
Conacher CG, Rossouw D, Bauer FFB (2019) Peer pressure: evolutionary responses to biotic pressures in wine yeasts. FEMS Yeast Res 19:1–12. https://doi.org/10.1093/femsyr/foz072
Costa OYA, Pijl A, Kuramae EE (2020) Dynamics of active potential bacterial and fungal interactions in the assimilation of acidobacterial EPS in soil. Soil Biol Biochem 148:107916. https://doi.org/10.1016/j.soilbio.2020.107916
Curiel JA, Morales P, Gonzalez R, Tronchoni J (2017) Different non-Saccharomyces yeast species stimulate nutrient consumption in S. cerevisiae mixed cultures. Front Microbiol 8:2121. https://doi.org/10.3389/fmicb.2017.02121
Dashkova V, Malashenkov D, Poulton N, Vorobjev I, Barteneva NS (2017) Imaging flow cytometry for phytoplankton analysis. Methods 112:188–200. https://doi.org/10.1016/j.ymeth.2016.05.007
Davey HM, Winson MK (2003) Using flow cytometry to quantify microbial heterogeneity. Curr Issues Mol Biol 5:9–15. https://doi.org/10.21775/cimb.005.009
David V, Terrat S, Herzine K, Claisse O, Masneuf-Pomarede I, Ranjard L, Alexandre H (2014) High - throughput sequencing of amplicons for monitoring yeast biodiversity in must and during alcoholic fermentation. J Ind Microbiol Biotechnol 41:811–821. https://doi.org/10.1007/s10295-014-1427-2
De Filippis F, La Storia A, Blaiotta G (2017) Monitoring the mycobiota during Greco di Tufo and Aglianico wine fermentation by 18S rRNA gene sequencing. Food Microbiol 63:117–122. https://doi.org/10.1016/j.fm.2016.11.010
De Roy K, Marzorati M, Van den Abbeele P, Van de Wiele T, Boon N (2014) Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities. Environ Microbiol 16:1472–1481. https://doi.org/10.1111/1462-2920.12343
Dey R, Rieger AM, Stephens C, Ashbolt NJ (2019) Interactions of Pseudomonas aeruginosa with Acanthamoeba polyphaga observed by imaging flow cytometry. Cytom Part A 95:555–564. https://doi.org/10.1002/cyto.a.23768
DiMucci DM (2020) Machine learning for microbial ecology: predicting interactions and identifying their putative mechanisms. Dissertation, Boston University.
Dolinšek J, Goldschmidt F, Johnson DR (2016) Synthetic microbial ecology and the dynamic interplay between microbial genotypes. FEMS Microbiol Rev 40:961–979. https://doi.org/10.1093/femsre/fuw024
du Toit SC, Rossouw D, du Toit M, Bauer FF (2020) Enforced mutualism leads to improved cooperative behavior between Saccharomyces cerevisiae and Lactobacillus plantarum. Microorganisms 8:1109. https://doi.org/10.3390/microorganisms8081109
Du Z-Y, Zienkiewicz K, Vande Pol N, Ostrom NE, Benning C, Bonito GM (2019) Algal-fungal symbiosis leads to photosynthetic mycelium. Elife 8:1–22. https://doi.org/10.7554/elife.47815
Dujon BA, Louis EJ (2017) Genome diversity and evolution in the budding yeasts (Saccharomycotina). Genetics 206:717–750. https://doi.org/10.1534/genetics.116.199216
Dukovski I, Bajić D, Chacón JM, Quintin M, Vila JC, Sulheim S, Pacheco AR, Bernstein DB, Rieh WJ, Korolev KS, Sanchez A, Harcombe WR, Segrè D (2020) Computation Of Microbial Ecosystems in Time and Space (COMETS): an open source collaborative platform for modeling ecosystems metabolism. arXiv Quant Methods
Dunham MJ (2007) Synthetic ecology: a model system for cooperation. Proc Natl Acad Sci U S A 104:1741–1742. https://doi.org/10.1073/pnas.0611067104
Dunker S (2019) Hidden secrets behind dots: improved phytoplankton taxonomic resolution using high-throughput imaging flow cytometry. Cytom Part A 95:854–868. https://doi.org/10.1002/cyto.a.23870
Englezos V, Cachón DC, Rantsiou K, Blanco P, Petrozziello M, Pollon M, Giacosa S, Río Segade S, Rolle L, Cocolin L (2019a) Effect of mixed species alcoholic fermentation on growth and malolactic activity of lactic acid bacteria. Appl Microbiol Biotechnol 103:7687–7702. https://doi.org/10.1007/s00253-019-10064-1
Englezos V, Cravero F, Torchio F, Rantsiou K, Ortiz-Julien A, Lambri M, Gerbi V, Rolle L, Cocolin L (2018) Oxygen availability and strain combination modulate yeast growth dynamics in mixed culture fermentations of grape must with Starmerella bacillaris and Saccharomyces cerevisiae. Food Microbiol 69:179–188. https://doi.org/10.1016/j.fm.2017.08.007
Englezos V, Pollon M, Rantsiou K, Ortiz-Julien A, Botto R, Río Segade S, Giacosa S, Rolle L, Cocolin L (2019b) Saccharomyces cerevisiae-Starmerella bacillaris strains interaction modulates chemical and volatile profile in red wine mixed fermentations. Food Res Int 122:392–401. https://doi.org/10.1016/j.foodres.2019.03.072
Englezos V, Rantsiou K, Giacosa S, Río Segade S, Rolle L, Cocolin L (2019c) Cell-to-cell contact mechanism modulates Starmerella bacillaris death in mixed culture fermentations with Saccharomyces cerevisiae. Int J Food Microbiol 289:106–114. https://doi.org/10.1016/j.ijfoodmicro.2018.09.009
Faassen S, Hitzmann B (2015) Fluorescence spectroscopy and chemometric modeling for bioprocess monitoring. Sensors 15:10271–10291. https://doi.org/10.3390/s150510271
Fiegna F, Moreno-Letelier A, Bell T, Barraclough TG (2015) Evolution of species interactions determines microbial community productivity in new environments. ISME J 9:1235–1245. https://doi.org/10.1038/ismej.2014.215
Fleet GH (2003) Yeast interactions and wine flavour. Int J Food Microbiol 86:11–22. https://doi.org/10.1016/S0168-1605(03)00245-9
Frankowiak K, Wang XT, Sigman DM, Gothmann AM, Kitahara MV, Mazur M, Meibom A, Stolarski J (2016) Photosymbiosis and the expansion of shallow-water corals. Sci Adv 2:e1601122. https://doi.org/10.1126/sciadv.1601122
Friman V-P, Hiltunen T, Laakso J, Kaitala V (2008) Availability of prey resources drives evolution of predator–prey interaction. Proc R Soc B Biol Sci 275:1625–1633. https://doi.org/10.1098/rspb.2008.0174
Germerodt S, Bohl K, Lück A, Pande S, Schröter A, Kaleta C, Schuster S, Kost C (2016) Pervasive selection for cooperative cross-feeding in bacterial communities. PLoS Comput Biol 12:1–21. https://doi.org/10.1371/journal.pcbi.1004986
Geva-Zatorsky N, Alvarez D, Hudak JE, Reading NC, Erturk-Hasdemir D, Dasgupta S, Von Andrian UH, Kasper DL (2015) In vivo imaging and tracking of host-microbiota interactions via metabolic labeling of gut anaerobic bacteria. Nat Med 21:1091–1100. https://doi.org/10.1038/nm.3929
Gorter FA, Manhart M, Ackermann M (2020) Understanding the evolution of interspecies interactions in microbial communities. Philos Trans R Soc B Biol Sci 375:20190256. https://doi.org/10.1098/rstb.2019.0256
Grangeteau C, Roullier-Gall C, Rousseaux S, Gougeon RD, Schmitt-Kopplin P, Alexandre H, Guilloux-Benatier M (2017) Wine microbiology is driven by vineyard and winery anthropogenic factors. Microb Biotechnol 10:354–370. https://doi.org/10.1111/1751-7915.12428
Guillamón JM, Barrio E (2017) Genetic polymorphism in wine yeasts: mechanisms and methods for its detection. Front Microbiol 8:1–20. https://doi.org/10.3389/fmicb.2017.00806
Hart SFM, Skelding D, Waite AJ, Burton JC, Shou W (2019) High-throughput quantification of microbial birth and death dynamics using fluorescence microscopy. Quant Biol 7:69–81. https://doi.org/10.1007/s40484-018-0160-7
Hays SG, Patrick WG, Ziesack M, Oxman N, Silver PA (2015) Better together: engineering and application of microbial symbioses. Curr Opin Biotechnol 36:40–49. https://doi.org/10.1016/j.copbio.2015.08.008
Heins AL, Weuster-Botz D (2018) Population heterogeneity in microbial bioprocesses: origin, analysis, mechanisms, and future perspectives. Bioprocess Biosyst Eng 41:889–916. https://doi.org/10.1007/s00449-018-1922-3
Herron MD, Borin JM, Boswell JC, Walker J, Chen I-CK, Knox CA, Boyd M, Rosenzweig F, Ratcliff WC (2019) De novo origins of multicellularity in response to predation. Sci Rep 9:2328. https://doi.org/10.1038/s41598-019-39558-8
Heyse J, Buysschaert B, Props R, Rubbens P, Skirtach AG, Waegeman W, Boon N (2019) Coculturing bacteria leads to reduced phenotypic heterogeneities. Appl Environ Microbiol 85:1–13. https://doi.org/10.1128/AEM.02814-18
Higuchi-sanabria R, Garcia EJ, Tomoiaga D, Munteanu EL (2016) Characterization of fluorescent proteins for three- and four-color live-cell imaging in S. cerevisiae. PLoS One 11:1–15. https://doi.org/10.1371/journal.pone.0146120
Hillesland KL (2018) Evolution on the bright side of life: microorganisms and the evolution of mutualism. Ann N Y Acad Sci 1422:88–103. https://doi.org/10.1111/nyas.13515
Hillesland KL, Stahl DA (2010) Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc Natl Acad Sci U S A 107:2124–2129. https://doi.org/10.1073/pnas.0908456107
Hom EFY, Murray AW (2014) Plant-fungal ecology. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345:94–98. https://doi.org/10.1126/science.1253320
Johns NI, Blazejewski T, Gomes ALC, Wang HH (2016) Principles for designing synthetic microbial communities. Curr Opin Microbiol 31:146–153. https://doi.org/10.1016/j.mib.2016.03.010
Kaitala V, Hiltunen T, Becks L, Scheuerl T (2020) Co-evolution as an important component explaining microbial predator-prey interaction. J Theor Biol 486:110095. https://doi.org/10.1016/j.jtbi.2019.110095
Kazamia E, Aldridge DC, Smith AG (2012a) Synthetic ecology - a way forward for sustainable algal biofuel production? J Biotechnol 162:163–169. https://doi.org/10.1016/j.jbiotec.2012.03.022
Kazamia E, Czesnick H, Van Nguyen TT, Croft MT, Sherwood E, Sasso S, Hodson SJ, Warren MJ, Smith AG (2012b) Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation. Environ Microbiol 14:1466–1476. https://doi.org/10.1111/j.1462-2920.2012.02733.x
Kecskeméti E, Berkelmann-Löhnertz B, Reineke A (2016) Are epiphytic microbial communities in the carposphere of ripening grape clusters (Vitis vinifera L.) different between conventional, organic, and biodynamic grapes? PLoS One 11:1–23. https://doi.org/10.1371/journal.pone.0160852
Kemsawasd V, Branco P, Almeida MG, Caldeira J, Albergaria H, Arneborg N (2015) Cell-to-cell contact and antimicrobial peptides play a combined role in the death of Lachanchea thermotolerans during mixed-culture alcoholic fermentation with Saccharomyces cerevisiae. FEMS Microbiol Lett 362:1–8. https://doi.org/10.1093/femsle/fnv103
Kioroglou D, Kraeva-Deloire E, Schmidtke LM, Mas A, Portillo MC (2019) Geographical origin has a greater impact on grape berry fungal community than grape variety and maturation state. Microorganisms 7:9–14. https://doi.org/10.3390/microorganisms7120669
Knight R, Callewaert C, Marotz C, Hyde ER, Debelius JW, McDonald D, Sogin ML (2017) The microbiome and human biology. Annu Rev Genomics Hum Genet 18:65–86. https://doi.org/10.1146/annurev-genom-083115-022438
Knight S, Goddard MR (2014) Quantifying separation and similarity in a Saccharomyces cerevisiae metapopulation. ISME J 9:361–370. https://doi.org/10.1038/ismej.2014.132
Knight S, Klaere S, Fedrizzi B, Goddard MR (2015) Regional microbial signatures positively correlate with differential wine phenotypes: evidence for a microbial aspect to terroir. Nat Sci Reports 5:14233. https://doi.org/10.1038/srep14233
Knight SJ, Karon O, Goddard MR (2020) Small scale fungal community differentiation in a vineyard system. Food Microbiol 87:103358. https://doi.org/10.1016/j.fm.2019.103358
König JC, Steinwedel T, Solle D, Lindner P, De Vries I, Hentrop T, Findeis M, John GT, Scheper T, Beutel S (2018) Development and characterisation of a new fluorescence sensor for online monitoring of bioprocesses. J Sensors Sens Syst 7:461–467. https://doi.org/10.5194/jsss-7-461-2018
Kron P, Suda J, Husband BC (2007) Applications of flow cytometry to evolutionary and population biology. Annu Rev Ecol Evol Syst 38:847–876. https://doi.org/10.1146/annurev.ecolsys.38.091206.095504
La Sarre B, McCully AL, Lennon JT, McKinlay JB (2017) Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients. ISME J 11:337–348. https://doi.org/10.1038/ismej.2016.141
Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB (2012) Species interactions alter evolutionary responses to a novel environment. PLoS Biol 10:1001330. https://doi.org/10.1371/journal.pbio.1001330
Lee S, Lim WA, Thorn KS (2013) Improved blue, green, and red fluorescent protein tagging vectors for S. cerevisiae. PLoS One 8:1–8. https://doi.org/10.1371/journal.pone.0067902
Legras JL, Galeote V, Bigey F, Camarasa C, Marsit S, Nidelet T, Sanchez I, Couloux A, Guy J, Franco-Duarte R, Marcet-Houben M, Gabaldon T, Schuller D, Sampaio JP, Dequin S (2018) Adaptation of S. cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication. Mol Biol Evol 35:1712–1727. https://doi.org/10.1093/molbev/msy066
Li T, Li C-T, Butler K, Hays SG, Guarnieri MT, Oyler GA, Betenbaugh MJ (2017) Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform. Biotechnol Biofuels 10:55. https://doi.org/10.1186/s13068-017-0736-x
Liao C, Wang T, Maslov S, Xavier JB (2020) Modeling microbial cross-feeding at intermediate scale portrays community dynamics and species coexistence. PLOS Comput Biol 16:e1008135. https://doi.org/10.1371/journal.pcbi.1008135
Lindemann SR, Bernstein HC, Song H, Fredrickson JK, Fields MW, Shou W, Johnson DR, Beliaev AS (2016) Engineering microbial consortia for controllable outputs. ISME 10:2077–2084. https://doi.org/10.1038/ismej.2016.26
Little AEF, Robinson CJ, Peterson SB, Raffa KF, Handelsman J (2008) Rules of engagement: interspecies interactions that regulate microbial communities. Annu Rev Microbiol 62:375–401. https://doi.org/10.1146/annurev.micro.030608.101423
Liu D, Chen Q, Zhang P, Chen D, Howell KS (2020) The fungal microbiome is an important component of vineyard ecosystems and correlates with regional distinctiveness of wine. mSphere 5:e00534-20. https://doi.org/10.1128/mSphere.00534-20
Liu Y, Rousseaux S, Tourdot-Maréchal R, Sadoudi M, Gougeon R, Schmitt-Kopplin P, Alexandre H (2017) Wine microbiome: a dynamic world of microbial interactions. Crit Rev Food Sci Nutr 57:856–873. https://doi.org/10.1080/10408398.2014.983591
Liu Z, Cichocki N, Bonk F, Günther S, Schattenberg F, Harms H, Centler F, Müller S (2018) Ecological stability properties of microbial communities assessed by flow cytometry. mSphere 3:e00564-17. https://doi.org/10.1128/mSphere.00564-17
Liu Z, Müller S (2020) Bacterial community diversity dynamics highlight degrees of nestedness and turnover patterns. Cytom Part A 97:742–748. https://doi.org/10.1002/cyto.a.23965
Lleixà J, Kioroglou D, Mas A, Portillo M d C (2018) Microbiome dynamics during spontaneous fermentations of sound grapes in comparison with sour rot and Botrytis infected grapes. Int J Food Microbiol 281:36–46. https://doi.org/10.1016/j.ijfoodmicro.2018.05.016
Longin C, Petitgonnet C, Guilloux-Benatier M, Rousseaux S, Alexandre H (2017) Application of flow cytometry to wine microorganisms. Food Microbiol 62:221–231. https://doi.org/10.1016/j.fm.2016.10.023
Lopez CLF, Beaufort S, Brandam C, Taillandier P (2014) Interactions between Kluyveromyces marxianus and Saccharomyces cerevisiae in tequila must type medium fermentation. World J Microbiol Biotechnol 30:2223–2229. https://doi.org/10.1007/s11274-014-1643-y
Lourenço ND, Lopes JA, Almeida CF, Sarraguça MC, Pinheiro HM (2012) Bioreactor monitoring with spectroscopy and chemometrics: a review. Anal Bioanal Chem 404:1211–1237. https://doi.org/10.1007/s00216-012-6073-9
Lukumbuzya M, Schmid M, Pjevac P, Daims H (2019) A multicolor fluorescence in situ hybridization approach using an extended set of fluorophores to visualize microorganisms. Front Microbiol 10:1–13. https://doi.org/10.3389/fmicb.2019.01383
Marsit S, Leducq JB, Durand É, Marchant A, Filteau M, Landry CR (2017) Evolutionary biology through the lens of budding yeast comparative genomics. Nat Rev Genet 18:581–598. https://doi.org/10.1038/nrg.2017.49
Marsland R, Cui W, Goldford J, Mehta P (2020) The Community Simulator: a Python package for microbial ecology. PLoS One 15:1–18. https://doi.org/10.1371/journal.pone.0230430
Mattanovich D, Borth N (2006) Applications of cell sorting in biotechnology. Microb Cell Fact 5:1–11. https://doi.org/10.1186/1475-2859-5-12
McFall-Ngai M (2014) Divining the essence of symbiosis: insights from the squid-vibrio model. PLoS Biol 12:e1001783. https://doi.org/10.1371/journal.pbio.1001783
Mencher A, Morales P, Valero E, Tronchoni J, Patil KR, Gonzalez R (2020) Proteomic characterization of extracellular vesicles produced by several wine yeast species. Microb Biotechnol 13:1581–1596. https://doi.org/10.1111/1751-7915.13614
Momeni B, Brileya KA, Fields MW, Shou W (2013) Strong inter-population cooperation leads to partner intermixing in microbial communities. Elife 2:1–23. https://doi.org/10.7554/eLife.00230
Morgan HH, du Toit M, Setati ME (2017) The grapevine and wine microbiome: Insights from high-throughput amplicon sequencing. Front. Microbiol. 8:820. https://doi.org/10.3389/fmicb.2017.00820
Morrison-Whittle P, Goddard MR (2018) From vineyard to winery: a source map of microbial diversity driving wine fermentation. Environ Microbiol 20:75–84. https://doi.org/10.1111/1462-2920.13960
Morrison-Whittle P, Lee SA, Goddard MR (2017) Fungal communities are differentially affected by conventional and biodynamic agricultural management approaches in vineyard ecosystems. Agric Ecosyst Environ 246:306–313. https://doi.org/10.1016/j.agee.2017.05.022
Naidoo RK, Simpson ZF, Oosthuizen JR, Bauer FF (2019) Nutrient exchange of carbon and nitrogen promotes the formation of stable mutualisms between Chlorella sorokiniana and Saccharomyces cerevisiae under engineered synthetic growth conditions. Front Microbiol 10:1–16. https://doi.org/10.3389/fmicb.2019.00609
Nissen P, Arneborg N (2003) Characterization of early deaths of non-Saccharomyces yeasts in mixed cultures with Saccharomyces cerevisiae. Arch Microbiol 180:257–263. https://doi.org/10.1007/s00203-003-0585-9
Nissen P, Nielsen D, Arneborg N (2003) Viable Saccharomyces cerevisiae cells at high concentrations cause early growth arrest of non-Saccharomyces yeasts in mixed cultures by a cell-cell contact-mediated mechanism. Yeast 20:331–341. https://doi.org/10.1002/yea.965
Oosthuizen JR, Naidoo RK, Rossouw D, Bauer FF (2020) Evolution of mutualistic behaviour between Chlorella sorokiniana and Saccharomyces cerevisiae within a synthetic environment. J Ind Microbiol Biotechnol 47:357–372. https://doi.org/10.1007/s10295-020-02280-w
Pallmann CL, Brown JA, Olineka TL, Cocolin L, Mills DA, Bisson LF (2001) Use of WL medium to profile native flora fermentations. Am J Enol Vitic 52:198–203
Peng C, Andersen B, Arshid S, Larsen MR, Albergaria H, Lametsch R, Arneborg N (2019) Proteomics insights into the responses of Saccharomyces cerevisiae during mixed-culture alcoholic fermentation with Lachancea thermotolerans. FEMS Microbiol Ecol 95:1–16. https://doi.org/10.1093/femsec/fiz126
Peng X, Gilmore SP, O’Malley MA (2016) Microbial communities for bioprocessing: lessons learned from nature. Curr Opin Chem Eng 14:103–109. https://doi.org/10.1016/j.coche.2016.09.003
Pérez-Torrado R, Rantsiou K, Perrone B, Navarro-Tapia E, Querol A, Cocolin L (2017) Ecological interactions among Saccharomyces cerevisiae strains: insight into the dominance phenomenon. Sci Rep 7:1–10. https://doi.org/10.1038/srep43603
Petitgonnet C, Klein GL, Roullier-Gall C, Schmitt-Kopplin P, Quintanilla-Casas B, Vichi S, Julien-David D, Alexandre H (2019) Influence of cell-cell contact between L. thermotolerans and S. cerevisiae on yeast interactions and the exo-metabolome. Food Microbiol 83:122–133. https://doi.org/10.1016/j.fm.2019.05.005
Pinto C, Pinho D, Cardoso R, Custodio V, Fernandes J, Sousa S, Pinheiro M, Egas C, Gomes AC (2015) Wine fermentation microbiome: a landscape from different Portuguese wine appellations. Front Microbiol 6:905. https://doi.org/10.3389/fmicb.2015.00905
Ponomarova O, Gabrielli N, Sévin DC, Mülleder M, Zirngibl K, Bulyha K, Andrejev S, Kafkia E, Typas A, Sauer U, Ralser M, Patil KR (2017) Yeast creates a niche for symbiotic lactic acid bacteria through nitrogen overflow. Cell Syst 5:345–357.e6. https://doi.org/10.1016/j.cels.2017.09.002
Porter P, Deere D, Hardman M, Edward C, Pickup R (1997) Go with the flow - use of flow cytometry in environmental microbiology. FEMS Microbiol Ecol 24:93–101
Portillo M d C, Franquès J, Araque I, Reguant C, Bordons A (2016) Bacterial diversity of Grenache and Carignan grape surface from different vineyards at Priorat wine region (Catalonia, Spain). Int J Food Microbiol 219:56–63. https://doi.org/10.1016/j.ijfoodmicro.2015.12.002
Portillo M d C, Mas A (2016) Analysis of microbial diversity and dynamics during wine fermentation of Grenache grape variety by high-throughput barcoding sequencing. LWT- Food Sci Technol 72:317–321. https://doi.org/10.1016/j.lwt.2016.05.009
Props R, Monsieurs P, Mysara M, Clement L, Boon N (2016) Measuring the biodiversity of microbial communities by flow cytometry. Methods Ecol Evol 7:1376–1385. https://doi.org/10.1111/2041-210X.12607
Prosser JI (2020) Putting science back into microbial ecology: a question of approach. Philos Trans R Soc B Biol Sci 375:20190240. https://doi.org/10.1098/rstb.2019.0240
Prosser JI, Martiny JBH (2020) Conceptual challenges in microbial community ecology. Philos Trans R Soc B Biol Sci 375:2–4. https://doi.org/10.1098/rstb.2019.0241
Qian X, Chen L, Sui Y, Chen C, Zhang W, Zhou J, Dong W, Jiang M, Xin F, Ochsenreither K (2020) Biotechnological potential and applications of microbial consortia. Biotechnol Adv 40:107500. https://doi.org/10.1016/j.biotechadv.2019.107500
Renault PE, Albertin W, Bely M (2013) An innovative tool reveals interaction mechanisms among yeast populations under oenological conditions. Appl Microbiol Biotechnol 97:4105–4119. https://doi.org/10.1007/s00253-012-4660-5
Roell GW, Zha J, Carr RR, Koffas MA, Fong SS, Tang YJ (2019) Engineering microbial consortia by division of labor. Microb Cell Fact 18:1–11. https://doi.org/10.1186/s12934-019-1083-3
Roullier-Gall C, David V, Hemmler D, Schmitt-Kopplin P, Alexandre H (2020) Exploring yeast interactions through metabolic profiling. Sci Rep 10:1–10. https://doi.org/10.1038/s41598-020-63182-6
Rubbens P (2019) Machine learning approaches for microbial flow cytometry at the single-cell and community level. Dissertation, Ghent University.
Rubbens P, Props R (2021) Computational analysis of microbial flow cytometry data. mSystems 6:1–12. https://doi.org/10.1128/msystems.00895-20
Said SB, Or D (2017) Synthetic microbial ecology: engineering habitats for modular consortia. Front Microbiol 8:1125. https://doi.org/10.3389/fmicb.2017.01125
Sanchez A (2019) Defining higher-order interactions in synthetic ecology: lessons from physics and quantitative genetics. Cell Syst 9:519–520. https://doi.org/10.1016/j.cels.2019.11.009
Sanchez-Gorostiaga A, Bajić D, Osborne ML, Poyatos JF, Sanchez A (2019) High-order interactions distort the functional landscape of microbial consortia. PLOS Biol 17:e3000550. https://doi.org/10.1371/journal.pbio.3000550
Schäpper D, Alam MNHZ, Szita N, Eliasson Lantz A, Gernaey KV (2009) Application of microbioreactors in fermentation process development: a review. Anal Bioanal Chem 395:679–695. https://doi.org/10.1007/s00216-009-2955-x
Setati ME, Jacobson D, Bauer FF (2015) Sequence-based analysis of the Vitis vinifera L . cv Cabernet Sauvignon grape must mycobiome in three south african vineyards employing distinct agronomic systems. Front Microbiol 6:1358. https://doi.org/10.3389/fmicb.2015.01358
Sheff MA, Thorn KS (2004) Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21:661–670. https://doi.org/10.1002/yea.1130
Shekhawat K, Patterton H, Bauer FF, Setati ME (2019) RNA-seq based transcriptional analysis of Saccharomyces cerevisiae and Lachancea thermotolerans in mixed-culture fermentations under anaerobic conditions. BMC Genomics 20:1–15. https://doi.org/10.1186/s12864-019-5511-x
Stenuit B, Agathos SN (2015) Deciphering microbial community robustness through synthetic ecology and molecular systems synecology. Curr Opin Biotechnol 33:305–317. https://doi.org/10.1016/j.copbio.2015.03.012
Suzzi G, Schirone M, Sergi M, Marianella RM, Fasoli G, Aguzzi I, Tofalo R (2012) Multistarter from organic viticulture for red wine Montepulciano d’Abruzzo production. Front Microbiol 3:1–10. https://doi.org/10.3389/fmicb.2012.00135
Taillandier P, Lai QP, Julien-Ortiz A, Brandam C (2014) Interactions between Torulaspora delbrueckii and Saccharomyces cerevisiae in wine fermentation: influence of inoculation and nitrogen content. World J Microbiol Biotechnol 30:1959–1967. https://doi.org/10.1007/s11274-014-1618-z
Taylor MW, Tsai P, Anfang N, Ross HA, Goddard MR (2014) Pyrosequencing reveals regional differences in fruit-associated fungal communities. Environ Microbiol 16:2848–2858. https://doi.org/10.1111/1462-2920.12456
Tronchoni J, Curiel JA, Morales P, Torres-Pérez R, Gonzalez R (2017) Early transcriptional response to biotic stress in mixed starter fermentations involving Saccharomyces cerevisiae and Torulaspora delbrueckii. Int J Food Microbiol 241:60–68. https://doi.org/10.1016/j.ijfoodmicro.2016.10.017
Tsoi R, Dai Z, You L (2019) Emerging strategies for engineering microbial communities. Biotechnol Adv 37:107372. https://doi.org/10.1016/j.biotechadv.2019.03.011
Varela C, Schmidt SA, Borneman AR, Pang CNI, Krömerx JO, Khan A, Song X, Hodson MP, Solomon M, Mayr CM, Hines W, Pretorius IS, Baker MS, Roessner U, Mercurio M, Henschke PA, Wilkins MR, Chambers PJ (2018) Systems-based approaches enable identification of gene targets which improve the flavour profile of low-ethanol wine yeast strains. Metab Eng 49:178–191. https://doi.org/10.1016/j.ymben.2018.08.006
Volpi EV, Bridger JM (2008) FISH glossary: an overview of the fluorescence in situ hybridization technique. Biotechniques 45:385–409. https://doi.org/10.2144/000112811
Wang B, Wang Z, Chen T, Zhao X (2020) Development of novel bioreactor control systems based on smart sensors and actuators. Front Bioeng Biotechnol 8:1–15. https://doi.org/10.3389/fbioe.2020.00007
Wang C, Esteve-Zarzoso B, Mas A (2014) Monitoring of Saccharomyces cerevisiae, Hanseniaspora uvarum, and Starmerella bacillaris (synonym Candida zemplinina) populations during alcoholic fermentation by fluorescence in situ hybridization. Int J Food Microbiol 191:1–9. https://doi.org/10.1016/j.ijfoodmicro.2014.08.014
Wang C, García-fernández D, Mas A, Esteve-zarzoso B (2015a) Fungal diversity in grape must and wine fermentation assessed by massive sequencing, quantitative PCR and DGGE. Front Microbiol 6:1156. https://doi.org/10.3389/fmicb.2015.01156
Wang C, Mas A, Esteve-Zarzoso B (2015b) Interaction between Hanseniaspora uvarum and Saccharomyces cerevisiae during alcoholic fermentation. Int J Food Microbiol 206:67–74. https://doi.org/10.1016/j.ijfoodmicro.2015.04.022
Wang C, Mas A, Esteve-Zarzoso B (2016) The interaction between Saccharomyces cerevisiae and non-Saccharomyces yeast during alcoholic fermentation is species and strain specific. Front Microbiol 7:1–11. https://doi.org/10.3389/fmicb.2016.00502
Widder S, Allen RJ, Pfeiffer T, Curtis TP, Wiuf C, Sloan WT, Cordero OX, Brown SP, Momeni B, Shou W, Kettle H, Flint HJ, Haas AF, Laroche B, Kreft JU, Rainey PB, Freilich S, Schuster S, Milferstedt K, Van Der Meer JR, Grobkopf T, Huisman J, Free A, Picioreanu C, Quince C, Klapper I, Labarthe S, Smets BF, Wang H, Soyer OS, Allison SD, Chong J, Lagomarsino MC, Croze OA, Hamelin J, Harmand J, Hoyle R, Hwa TT, Jin Q, Johnson DR, de Lorenzo V, Mobilia M, Murphy B, Peaudecerf F, Prosser JI, Quinn RA, Ralser M, Smith AG, Steyer JP, Swainston N, Tarnita CE, Trably E, Warren PB, Wilmes P (2016) Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J 10:2557–2568. https://doi.org/10.1038/ismej.2016.45
Xu W, Liu B, Wang C, Kong X (2020) Organic cultivation of grape affects yeast succession and wine sensory quality during spontaneous fermentation. LWT - Food Sci Technol 120:108894. https://doi.org/10.1016/j.lwt.2019.108894
Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich NA, Mills DA, Martin G, Taghavi S, van der Lelie D, Gilbert JA (2015) The soil microbiome influences grapevine-associated microbiota. mBio 6:1–10. https://doi.org/10.1128/mBio.02527-14
Zhang J, Wang ET, Singh RP, Guo C, Shang Y, Chen J, Liu C (2019) Grape berry surface bacterial microbiome: impact from the varieties and clones in the same vineyard from central China. J Appl Microbiol 126:204–214. https://doi.org/10.1111/jam.14124
Zhou N, Bottagisi S, Katz M, Schacherer J, Friedrich A, Gojkovic Z, Swamy KBS, Knecht W, Compagno C, Piškur J (2017a) Yeast–bacteria competition induced new metabolic traits through large-scale genomic rearrangements in Lachancea kluyveri. FEMS Yeast Res 17. https://doi.org/10.1093/femsyr/fox060
Zhou N, Katz M, Knecht W, Compagno C, Piškur J (2018) Genome dynamics and evolution in yeasts: a long-term yeast-bacteria competition experiment. PLoS One 13:1–16. https://doi.org/10.1371/journal.pone.0194911
Zhou N, Swamy KBS, Leu JY, McDonald MJ, Galafassi S, Compagno C, Piškur J (2017b) Coevolution with bacteria drives the evolution of aerobic fermentation in Lachancea kluyveri. PLoS One 12:1–19. https://doi.org/10.1371/journal.pone.0173318
Zhu X, Torija M-J, Mas A, Beltran G, Navarro Y (2021) Effect of a multistarter yeast inoculum on ethanol reduction and population dynamics in wine fermentation. Foods 10:623. https://doi.org/10.3390/foods10030623
Zomorrodi AR, Segrè D (2016) Synthetic ecology of microbes: mathematical models and applications. J Mol Biol 428:837–861. https://doi.org/10.1016/j.jmb.2015.10.019
Zuñiga C, Li CT, Yu G, Al-Bassam MM, Li T, Jiang L, Zaramela LS, Guarnieri M, Betenbaugh MJ, Zengler K (2019) Environmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communities. Nat Microbiol 4:2184–2191. https://doi.org/10.1038/s41564-019-0567-6
Zuñiga C, Li T, Guarnieri MT, Jenkins JP, Li CT, Bingol K, Kim YM, Betenbaugh MJ, Zengler K (2020) Synthetic microbial communities of heterotrophs and phototrophs facilitate sustainable growth. Nat Commun 11:2184–2191. https://doi.org/10.1038/s41467-020-17612-8
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The authors would like to thank the following funders for supporting this research: the National Research Foundation of South Africa through Grant numbers 83471 (SA Research Chair in Integrated Wine Science) to FFB and Grant number 118505 (Competitive Programme for Rated Researchers) to MES, and the Royal Society Future Leaders—Independent African Researchers (FLAIR) grant to DR.
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The manuscript was conceptualised by FFB, and all authors contributed to the initial draft. The draft was revised and collated into a manuscript by CGC. Figures were drawn by CGC, tables were drawn by NAL. All authors approved the final version of the manuscript.
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Conacher, C., Luyt, N., Naidoo-Blassoples, R. et al. The ecology of wine fermentation: a model for the study of complex microbial ecosystems. Appl Microbiol Biotechnol 105, 3027–3043 (2021). https://doi.org/10.1007/s00253-021-11270-6
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DOI: https://doi.org/10.1007/s00253-021-11270-6