Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions

Albright, Michaeline N.; Sevanto, Sanna; Gallegos-Graves, La Verne; Dunbar, John

doi:10.1128/mbio.02089-20

Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions

Journal Article · Tue Oct 27 00:00:00 EDT 2020 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.02089-20· OSTI ID:1690276

; Sevanto, Sanna; Gallegos-Graves, La Verne;

ABSTRACT Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context—propagule pressure (inoculation dose and frequency) and biotic interactions (composition of introduced and resident communities)—is unknown. We tested the effect of these factors in driving microbial composition and functioning following 12 microbial community invasions (e.g., introductions of many microbial invaders) in microcosms. Ecosystem functioning over a 30-day postinvasion period was assessed by measuring activity (respiration) and environment modification (dissolved organic carbon abundance). To test the dependence on environmental context, experiments were performed in two resource environments. In both environments, biotic interactions were more important than propagule pressure in driving microbial composition and community function, but the magnitude of effect varied by environment. Successful invaders comprised approximately 8% of the total number of operational taxonomic units (OTUs). Bacteria were better invaders than fungi, with average relative abundances of 7.4% ± 6.8% and 1.5% ± 1.4% of OTUs, respectively. Common bacterial invaders were associated with stress response traits. The most resilient bacterial and fungal families, in other words, those least impacted by invasions, were linked to antimicrobial resistance or production traits. Illuminating the principles that determine community composition and functioning following microbial invasions is key to efficient community engineering. IMPORTANCE With increasing frequency, humans are introducing new microbes into preexisting microbiomes to alter functioning. Example applications include modification of microflora in human guts for better health and those of soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved with a better understanding of microbial invasions. We conducted a microbial community invasion experiment to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1690276

Alternate ID(s):: OSTI ID: 1739971

Report Number(s):: LA-UR--19-27879; e02089-20

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 5 Vol. 11; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (90)

Biotic resistance shapes the influence of propagule pressure on invasion success in bacterial communities Jones, Matt L.; Ramoneda, Josep; Rivett, Damian W. Ecology, Vol. 98, Issue 7 https://doi.org/10.1002/ecy.1852	journal	May 2017
Microbial community engineering for biopolymer production from glycerol Moralejo-Gárate, Helena; Mar’atusalihat, Emily; Kleerebezem, Robbert Applied Microbiology and Biotechnology, Vol. 92, Issue 3 https://doi.org/10.1007/s00253-011-3359-3	journal	June 2011
Invasion resistance and persistence: established plants win, even with disturbance and high propagule pressure McGlone, Christopher M.; Sieg, Carolyn Hull; Kolb, Thomas E. Biological Invasions, Vol. 13, Issue 2 https://doi.org/10.1007/s10530-010-9806-8	journal	June 2010
Ecological niche and species traits: key drivers of regional plant invader assemblages Thuiller, Wilfried; Gassó, Núria; Pino, Joan Biological Invasions, Vol. 14, Issue 9 https://doi.org/10.1007/s10530-012-0206-0	journal	March 2012
Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis Mummey, Daniel L.; Rillig, Matthias C.; Holben, William E. Plant and Soil, Vol. 271, Issue 1-2 https://doi.org/10.1007/s11104-004-2066-6	journal	April 2005
Revision of Phaeosphaeriaceae Phookamsak, Rungtiwa; Liu, Jian-Kui; McKenzie, Eric H. C. Fungal Diversity, Vol. 68, Issue 1 https://doi.org/10.1007/s13225-014-0308-3	journal	September 2014
Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semi-arid Mediterranean area Caravaca, F.; Alguacil, M. M.; Figueroa, D. Forest Ecology and Management, Vol. 182, Issue 1-3 https://doi.org/10.1016/S0378-1127(03)00067-7	journal	September 2003
Prebiotics and synbiotics: towards the next generation Rastall, Robert A.; Maitin, Vatsala Current Opinion in Biotechnology, Vol. 13, Issue 5 https://doi.org/10.1016/S0958-1669(02)00365-8	journal	October 2002
Can bacterial interference prevent infection? Reid, Gregor; Howard, Jeffrey; Gan, Bing Siang Trends in Microbiology, Vol. 9, Issue 9 https://doi.org/10.1016/S0966-842X(01)02132-1	journal	September 2001
Microorganisms-based methods for harmful algal blooms control: A review Sun, Rui; Sun, Pengfei; Zhang, Jianhong Bioresource Technology, Vol. 248 https://doi.org/10.1016/j.biortech.2017.07.175	journal	January 2018
Sustainable wastewater treatment: How might microbial fuel cells contribute Oh, Sung T.; Kim, Jung Rae; Premier, Giuliano C. Biotechnology Advances, Vol. 28, Issue 6 https://doi.org/10.1016/j.biotechadv.2010.07.008	journal	November 2010
Post-Antibiotic Gut Mucosal Microbiome Reconstitution Is Impaired by Probiotics and Improved by Autologous FMT Suez, Jotham; Zmora, Niv; Zilberman-Schapira, Gili Cell, Vol. 174, Issue 6 https://doi.org/10.1016/j.cell.2018.08.047	journal	September 2018
Treating Clostridium difficile Infection With Fecal Microbiota Transplantation Bakken, Johan S.; Borody, Thomas; Brandt, Lawrence J. Clinical Gastroenterology and Hepatology, Vol. 9, Issue 12 https://doi.org/10.1016/j.cgh.2011.08.014	journal	December 2011
The role of arbuscular mycorrhizal fungi and cattle manure in the establishment of Tocoyena selloana Schum. in mined dune areas de Souza, Renata Gomes; Goto, Bruno Tomio; Alves da Silva, Danielle Karla European Journal of Soil Biology, Vol. 46, Issue 3-4 https://doi.org/10.1016/j.ejsobi.2010.04.004	journal	May 2010
Prebiotics and their long-term influence on the microbial populations of the mouse bowel Santos, A.; San Mauro, M.; Díaz, D. Marquina Food Microbiology, Vol. 23, Issue 5 https://doi.org/10.1016/j.fm.2005.07.004	journal	August 2006
Sphingolipids in host–microbial interactions Heaver, Stacey L.; Johnson, Elizabeth L.; Ley, Ruth E. Current Opinion in Microbiology, Vol. 43 https://doi.org/10.1016/j.mib.2017.12.011	journal	June 2018
A molecular approach to ascertain the success of “in situ” AM fungi inoculation in the revegetation of a semiarid, degraded land Alguacil, Maria del Mar; Torrecillas, Emma; Kohler, Josef Science of The Total Environment, Vol. 409, Issue 15 https://doi.org/10.1016/j.scitotenv.2011.04.029	journal	July 2011
Engineering microbial consortia: a new frontier in synthetic biology Brenner, Katie; You, Lingchong; Arnold, Frances H. Trends in Biotechnology, Vol. 26, Issue 9, p. 483-489 https://doi.org/10.1016/j.tibtech.2008.05.004	journal	September 2008
Interchange of entire communities: microbial community coalescence Rillig, Matthias C.; Antonovics, Janis; Caruso, Tancredi Trends in Ecology & Evolution, Vol. 30, Issue 8 https://doi.org/10.1016/j.tree.2015.06.004	journal	August 2015
Experimental Design and Data Analysis for Biologists Quinn, Gerry P.; Keough, Michael J. Cambridge University Press https://doi.org/10.1017/CBO9780511806384	book	January 2012
Fecal Microbiota Transplantation for Clostridium difficile Infection: Systematic Review and Meta-Analysis Kassam, Zain; Lee, Christine H.; Yuan, Yuhong American Journal of Gastroenterology, Vol. 108, Issue 4 https://doi.org/10.1038/ajg.2013.59	journal	January 2013
Examining the global distribution of dominant archaeal populations in soil Bates, Scott T.; Berg-Lyons, Donna; Caporaso, J. Gregory The ISME Journal, Vol. 5, Issue 5 https://doi.org/10.1038/ismej.2010.171	journal	November 2010
Erratum: The social structure of microbial community involved in colonization resistance He, Xuesong; McLean, Jeffrey S.; Guo, Lihong The ISME Journal, Vol. 8, Issue 11 https://doi.org/10.1038/ismej.2014.109	journal	October 2014
Temporal variation overshadows the response of leaf litter microbial communities to simulated global change Matulich, Kristin L.; Weihe, Claudia; Allison, Steven D. The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.58	journal	May 2015
Microbial legacies alter decomposition in response to simulated global change Martiny, Jennifer BH; Martiny, Adam C.; Weihe, Claudia The ISME Journal, Vol. 11, Issue 2 https://doi.org/10.1038/ismej.2016.122	journal	October 2016
Engineering microbial consortia for controllable outputs Lindemann, Stephen R.; Bernstein, Hans C.; Song, Hyun-Seob The ISME Journal, Vol. 10, Issue 9 https://doi.org/10.1038/ismej.2016.26	journal	March 2016
A conceptual framework for invasion in microbial communities Kinnunen, Marta; Dechesne, Arnaud; Proctor, Caitlin The ISME Journal, Vol. 10, Issue 12 https://doi.org/10.1038/ismej.2016.75	journal	May 2016
Biodiversity as a barrier to ecological invasion Kennedy, Theodore A.; Naeem, Shahid; Howe, Katherine M. Nature, Vol. 417, Issue 6889 https://doi.org/10.1038/nature00776	journal	June 2002
Microbial diversity drives multifunctionality in terrestrial ecosystems Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Reich, Peter B. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10541	journal	January 2016
Environmental conditions and community evenness determine the outcome of biological invasion De Roy, Karen; Marzorati, Massimo; Negroni, Andrea Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2392	journal	January 2013
Deterministic processes vary during community assembly for ecologically dissimilar taxa Powell, Jeff R.; Karunaratne, Senani; Campbell, Colin D. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9444	journal	October 2015
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche Mallon, C. A.; Le Roux, X.; van Doorn, G. S. The ISME Journal, Vol. 12, Issue 3 https://doi.org/10.1038/s41396-017-0003-y	journal	January 2018
Stochastic processes govern invasion success in microbial communities when the invader is phylogenetically close to resident bacteria Kinnunen, Marta; Dechesne, Arnaud; Albrechtsen, Hans-Jørgen The ISME Journal, Vol. 12, Issue 11 https://doi.org/10.1038/s41396-018-0202-1	journal	July 2018
Sphingolipids produced by gut bacteria enter host metabolic pathways impacting ceramide levels Johnson, Elizabeth L.; Heaver, Stacey L.; Waters, Jillian L. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16274-w	journal	May 2020
Cytochalasan and Tyrosine-Derived Alkaloids from the Marine Sediment-Derived Fungus Westerdykella dispersa and Their Bioactivities Xu, Dan; Luo, Minghe; Liu, Fenglou Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-12327-1	journal	September 2017
Interactions between predation and disturbances shape prey communities Karakoç, Canan; Radchuk, Viktoriia; Harms, Hauke Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-21219-x	journal	February 2018
Membrane sphingolipids as essential molecular signals for Bacteroides survival in the intestine An, D.; Na, C.; Bielawski, J. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1001501107	journal	September 2010
Microbial diversity determines the invasion of soil by a bacterial pathogen van Elsas, J. D.; Chiurazzi, M.; Mallon, C. A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 4 https://doi.org/10.1073/pnas.1109326109	journal	January 2012
Dynamics of an experimental microbial invasion Acosta, Francisco; Zamor, Richard M.; Najar, Fares Z. Proceedings of the National Academy of Sciences, Vol. 112, Issue 37 https://doi.org/10.1073/pnas.1505204112	journal	August 2015
Decomposition responses to climate depend on microbial community composition Glassman, Sydney I.; Weihe, Claudia; Li, Junhui Proceedings of the National Academy of Sciences, Vol. 115, Issue 47 https://doi.org/10.1073/pnas.1811269115	journal	November 2018
Toxicity drives facilitation between 4 bacterial species Piccardi, Philippe; Vessman, Björn; Mitri, Sara Proceedings of the National Academy of Sciences, Vol. 116, Issue 32 https://doi.org/10.1073/pnas.1906172116	journal	July 2019
Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Lenski, R. E.; Travisano, M. Proceedings of the National Academy of Sciences, Vol. 91, Issue 15 https://doi.org/10.1073/pnas.91.15.6808	journal	July 1994
PEAR: a fast and accurate Illumina Paired-End reAd mergeR Zhang, J.; Kobert, K.; Flouri, T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt593	journal	October 2013
A new fungal large subunit ribosomal RNA primer for high throughput sequencing surveys Mueller, Rebecca C.; Gallegos-Graves, La Verne; Kuske, Cheryl R. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fiv153	journal	December 2015
Resource availability modulates biodiversity‐invasion relationships by altering competitive interactions Yang, Tianjie; Wei, Zhong; Friman, Ville‐Petri Environmental Microbiology, Vol. 19, Issue 8 https://doi.org/10.1111/1462-2920.13708	journal	March 2017
Dispersal alters soil microbial community response to drought Evans, S. E.; Bell‐Dereske, L. P.; Dougherty, K. M. Environmental Microbiology, Vol. 22, Issue 3 https://doi.org/10.1111/1462-2920.14707	journal	July 2019
Biological invasion hotspots: a trait-based perspective reveals new sub-continental patterns Iannone, Basil V.; Potter, Kevin M.; Guo, Qinfeng Ecography, Vol. 39, Issue 10 https://doi.org/10.1111/ecog.01973	journal	December 2015
The community ecology of invasive species: where are we and what's next? Gallien, Laure; Carboni, Marta Ecography, Vol. 40, Issue 2 https://doi.org/10.1111/ecog.02446	journal	November 2016
Elevated success of multispecies bacterial invasions impacts community composition during ecological succession Rivett, Damian W.; Jones, Matt L.; Ramoneda, Josep Ecology Letters, Vol. 21, Issue 4 https://doi.org/10.1111/ele.12916	journal	February 2018
An experimental analysis of species sorting and mass effects in freshwater bacterioplankton Souffreau, Caroline; Pecceu, Bert; Denis, Carla Freshwater Biology, Vol. 59, Issue 10 https://doi.org/10.1111/fwb.12408	journal	July 2014
Diversity of locust gut bacteria protects against pathogen invasion Dillon, R. J.; Vennard, C. T.; Buckling, A. Ecology Letters, Vol. 8, Issue 12 https://doi.org/10.1111/j.1461-0248.2005.00828.x	journal	December 2005
Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems: Invasive microbes Litchman, Elena Ecology Letters, Vol. 13, Issue 12 https://doi.org/10.1111/j.1461-0248.2010.01544.x	journal	November 2010
Eight questions about invasions and ecosystem functioning Strayer, David L. Ecology Letters, Vol. 15, Issue 10 https://doi.org/10.1111/j.1461-0248.2012.01817.x	journal	June 2012
Bacterial diversity promotes community stability and functional resilience after perturbation Girvan, M. S.; Campbell, C. D.; Killham, K. Environmental Microbiology, Vol. 7, Issue 3 https://doi.org/10.1111/j.1462-2920.2005.00695.x	journal	March 2005
Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework Catford, Jane A.; Jansson, Roland; Nilsson, Christer Diversity and Distributions, Vol. 15, Issue 1 https://doi.org/10.1111/j.1472-4642.2008.00521.x	journal	January 2009
Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils Brown, Shawn P.; Jumpponen, Ari Molecular Ecology, Vol. 23, Issue 2 https://doi.org/10.1111/mec.12487	journal	September 2013
Do bacterial and fungal communities assemble differently during primary succession? Schmidt, S. K.; Nemergut, D. R.; Darcy, J. L. Molecular Ecology, Vol. 23, Issue 2 https://doi.org/10.1111/mec.12589	journal	January 2014
Sources of inocula influence mycorrhizal colonization of plants in restoration projects: a meta-analysis: Mycorrhizal inoculation in restoration Maltz, Mia R.; Treseder, Kathleen K. Restoration Ecology, Vol. 23, Issue 5 https://doi.org/10.1111/rec.12231	journal	June 2015
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Soil Bacterial and Fungal Communities Show Distinct Recovery Patterns during Forest Ecosystem Restoration Sun, Shan; Li, Song; Avera, Bethany N. Applied and Environmental Microbiology, Vol. 83, Issue 14 https://doi.org/10.1128/AEM.00966-17	journal	May 2017
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities Schloss, P. D.; Westcott, S. L.; Ryabin, T. Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541 https://doi.org/10.1128/AEM.01541-09	journal	October 2009
High Microbial Diversity Promotes Soil Ecosystem Functioning Maron, Pierre-Alain; Sarr, Amadou; Kaisermann, Aurore Applied and Environmental Microbiology, Vol. 84, Issue 9 https://doi.org/10.1128/AEM.02738-17	journal	February 2018
Role of Sphingolipids in Microbial Pathogenesis Heung, Lena J.; Luberto, Chiara; Del Poeta, Maurizio Infection and Immunity, Vol. 74, Issue 1 https://doi.org/10.1128/IAI.74.1.28-39.2006	journal	January 2006
From Structure to Function: the Ecology of Host-Associated Microbial Communities Robinson, C. J.; Bohannan, B. J. M.; Young, V. B. Microbiology and Molecular Biology Reviews, Vol. 74, Issue 3 https://doi.org/10.1128/MMBR.00014-10	journal	August 2010
Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Vilgalys, R.; Hester, M. Journal of Bacteriology, Vol. 172, Issue 8 https://doi.org/10.1128/jb.172.8.4238-4246.1990	journal	August 1990
Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species Kastman, Erik K.; Kamelamela, Noelani; Norville, Josh W. mBio, Vol. 7, Issue 5 https://doi.org/10.1128/mBio.01157-16	journal	October 2016
Broadscale Ecological Patterns Are Robust to Use of Exact Sequence Variants versus Operational Taxonomic Units Glassman, Sydney I.; Martiny, Jennifer B. H. mSphere, Vol. 3, Issue 4 https://doi.org/10.1128/mSphere.00148-18	journal	July 2018
Ecosystem Consequences of Biological Invasions Ehrenfeld, Joan G. Annual Review of Ecology, Evolution, and Systematics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev-ecolsys-102209-144650	journal	December 2010
The Role of Propagule Pressure in Biological Invasions Simberloff, Daniel Annual Review of Ecology, Evolution, and Systematics, Vol. 40, Issue 1 https://doi.org/10.1146/annurev.ecolsys.110308.120304	journal	December 2009
Shaping the oral microbiota through intimate kissing Kort, Remco; Caspers, Martien; van de Graaf, Astrid Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-41	journal	November 2014
Propagule pressure increase and phylogenetic diversity decrease community’s susceptibility to invasion Ketola, T.; Saarinen, K.; Lindström, L. BMC Ecology, Vol. 17, Issue 1 https://doi.org/10.1186/s12898-017-0126-z	journal	April 2017
Advances in industrial microbiome based on microbial consortium for biorefinery Jiang, Li-Li; Zhou, Jin-Jie; Quan, Chun-Shan Bioresources and Bioprocessing, Vol. 4, Issue 1 https://doi.org/10.1186/s40643-017-0141-0	journal	February 2017
Dissecting the null model for biological invasions: A meta-analysis of the propagule pressure effect Cassey, Phillip; Delean, Steven; Lockwood, Julie L. PLOS Biology, Vol. 16, Issue 4 https://doi.org/10.1371/journal.pbio.2005987	journal	April 2018
Bacterial Diversity Stabilizes Community Productivity Eisenhauer, Nico; Scheu, Stefan; Jousset, Alexandre PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0034517	journal	March 2012
Plants Probiotics as a Tool to Produce Highly Functional Fruits: The Case of Phyllobacterium and Vitamin C in Strawberries Flores-Félix, José David; Silva, Luis R.; Rivera, Lina P. PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0122281	journal	April 2015
Getting the Right Traits: Reproductive and Dispersal Characteristics Predict the Invasiveness of Herbaceous Plant Species Moravcová, Lenka; Pyšek, Petr; Jarošík, Vojtěch PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0123634	journal	April 2015
Effects of initial microbial biomass abundance on respiration during pine litter decomposition Albright, Michaeline B. N.; Runde, Andreas; Lopez, Deanna PLOS ONE, Vol. 15, Issue 2 https://doi.org/10.1371/journal.pone.0224641	journal	February 2020
Acetic Acid Bacteria in the Food Industry: Systematics, Characteristics and Applications Gomes, Rodrigo José; Borges, Maria de Fátima; Rosa, Morsyleide de Freitas Food Technology and Biotechnology, Vol. 56, Issue 2 https://doi.org/10.17113/ftb.56.02.18.5593	journal	January 2018
Testing the functional significance of microbial community composition Strickland, Michael S.; Lauber, Christian; Fierer, Noah Ecology, Vol. 90, Issue 2 https://doi.org/10.1890/08-0296.1	journal	February 2009
Microbial composition alters the response of litter decomposition to environmental change Matulich, Kristin L.; Martiny, Jennifer B. H. Ecology, Vol. 96, Issue 1 https://doi.org/10.1890/14-0357.1	journal	January 2015
Resource pulses can alleviate the biodiversity–invasion relationship in soil microbial communities Mallon, Cyrus A.; Poly, Franck; Le Roux, Xavier Ecology, Vol. 96, Issue 4 https://doi.org/10.1890/14-1001.1	journal	April 2015
Diazotrophic Endophytes of Poplar and Willow for Growth Promotion of Rice Plants in Nitrogen-Limited Conditions Kandel, S. L.; Herschberger, N.; Kim, S. H. Crop Science, Vol. 55, Issue 4 https://doi.org/10.2135/cropsci2014.08.0570	journal	July 2015
Phylogeny of Penicillium and the segregation of Trichocomaceae into three families Houbraken, J.; Samson, R. A. Studies in Mycology, Vol. 70 https://doi.org/10.3114/sim.2011.70.01	journal	September 2011
Microbial Community Coalescence for Microbiome Engineering Rillig, Matthias C.; Tsang, Alia; Roy, Julien Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01967	journal	December 2016
Soil Bacterial and Fungal Richness Forecast Patterns of Early Pine Litter Decomposition Albright, Michaeline B. N.; Johansen, Renee; Thompson, Jaron Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.542220	journal	November 2020
Microbial Consortia versus Single-Strain Inoculants: An Advantage in PGPM-Assisted Tomato Production? Bradáčová, Klára; Florea, Andrea; Bar-Tal, Asher Agronomy, Vol. 9, Issue 2 https://doi.org/10.3390/agronomy9020105	journal	February 2019
Plant probiotic bacteria: solutions to feed the world Menendez, Esther; Garcia-Fraile, Paula AIMS Microbiology, Vol. 3, Issue 3 https://doi.org/10.3934/microbiol.2017.3.502	journal	January 2017
Westerdykella reniformis sp. nov., producing the antibiotic metabolites melinacidin IV and chetracin B Ebead, Ghada A.; Overy, David P.; Berrué, Fabrice IMA Fungus, Vol. 3, Issue 2 https://doi.org/10.5598/imafungus.2012.03.02.11	journal	December 2012

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