Cooperative interactions between invader and resident microbial community members weaken the negative diversity-invasion relationship.
community ecology
cooperation
cooperative interactions
diversity‐invasion relationship
invasion resistance
microbial interactions
microbial invasion
Journal
Ecology letters
ISSN: 1461-0248
Titre abrégé: Ecol Lett
Pays: England
ID NLM: 101121949
Informations de publication
Date de publication:
May 2024
May 2024
Historique:
revised:
12
04
2024
received:
02
10
2023
accepted:
15
04
2024
medline:
7
5
2024
pubmed:
7
5
2024
entrez:
7
5
2024
Statut:
ppublish
Résumé
The negative diversity-invasion relationship observed in microbial invasion studies is commonly explained by competition between the invader and resident populations. However, whether this relationship is affected by invader-resident cooperative interactions is unknown. Using ecological and mathematical approaches, we examined the survival and functionality of Aminobacter niigataensis MSH1 to mineralize 2,6-dichlorobenzamide (BAM), a groundwater micropollutant affecting drinking water production, in sand microcosms when inoculated together with synthetic assemblies of resident bacteria. The assemblies varied in richness and in strains that interacted pairwise with MSH1, including cooperative and competitive interactions. While overall, the negative diversity-invasion relationship was retained, residents engaging in cooperative interactions with the invader had a positive impact on MSH1 survival and functionality, highlighting the dependency of invasion success on community composition. No correlation existed between community richness and the delay in BAM mineralization by MSH1. The findings suggest that the presence of cooperative residents can alleviate the negative diversity-invasion relationship.
Substances chimiques
Benzamides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
e14433Subventions
Organisme : EU FP7
ID : 266039
Organisme : Fonds Wetenschappelijk Onderzoek
ID : G0D0322N
Organisme : Belgian Science Policy (BELSPO)
ID : BELSPO P7/25
Informations de copyright
© 2024 John Wiley & Sons Ltd.
Références
Albers, C.N., Ellegaard‐Jensen, L., Harder, C.B., Rosendahl, S., Knudsen, B.E., Ekelund, F. et al. (2015) Groundwater chemistry determines the prokaryotic community structure of waterworks sand filters. Environmental Science & Technology, 49, 839–846.
Albers, C.N., Feld, L., Ellegaard‐Jensen, L. & Aamand, J. (2015) Degradation of trace concentrations of the persistent groundwater pollutant 2,6‐dichlorobenzamide (BAM) in bioaugmented rapid sand filters. Water Research, 83, 61–70.
Albright, M.B.N., Louca, S., Winkler, D.E., Feeser, K.L., Haig, S.‐J., Whiteson, K.L. et al. (2022) Solutions in microbiome engineering: prioritizing barriers to organism establishment. ISME Journal, 16, 331–338.
Allesina, S. & Levine, J.M. (2011) A competitive network theory of species diversity. Proceedings of the National Academy of Sciences, 108, 5638–5642.
Cohen, I., Huang, Y., Chen, J. & Benesty, J. (2009) Noise reduction in speech processing. Springer Berlin Heidelberg, Berlin, Heidelberg: Springer Topics in Signal Processing.
Colbourn, C.J. & McClary, D.W. (2008) Locating and detecting arrays for interaction faults. Journal of Combinatorial Optimization, 15, 17–48.
Cook, K.L., Garland, J.L., Layton, A.C., Dionisi, H.M., Levine, L.H. & Sayler, G.S. (2006) Effect of microbial species richness on community stability and community function in a model plant‐based wastewater processing system. Microbial Ecology, 52, 725–737.
Davis, M.A., Grime, J.P. & Thompson, K. (2000) Fluctuating resources in plant communities: a general theory of invasibility. Journal of Ecology, 88, 528–534.
De Roy, K., Marzorati, M., Negroni, A., Thas, O., Balloi, A., Fava, F. et al. (2013) Environmental conditions and community evenness determine the outcome of biological invasion. Nature Communications, 4, 1383.
Dejonghe, W., Berteloot, E., Goris, J., Boon, N., Crul, K., Maertens, S. et al. (2003) Synergistic degradation of linuron by a bacterial consortium and isolation of a single linuron‐degrading Variovorax strain. Applied and Environmental Microbiology, 69, 1532–1541.
Duan, K., Dammel, C., Stein, J., Rabin, H. & Surette, M.G. (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Molecular Microbiology, 50, 1477–1491.
Eisenhauer, N., Schulz, W., Scheu, S. & Jousset, A. (2013) Niche dimensionality links biodiversity and invasibility of microbial communities. Functional Ecology, 27, 282–288.
Ellegaard‐Jensen, L., Albers, C.N. & Aamand, J. (2016) Protozoa graze on the 2,6‐dichlorobenzamide (BAM)‐degrading bacterium Aminobacter sp. MSH1 introduced into waterworks sand filters. Applied Microbiology and Biotechnology, 100, 8965–8973.
Elton, C.S. (1958) The ecology of invasions by animals and plants. US, Boston, Massachusetts: Springer.
Fargione, J.E. & Tilman, D. (2005) Diversity decreases invasion via both sampling and complementarity effects. Ecology Letters, 8, 604–611.
Ferreira, D.A., da Silva, T.F., Pylro, V.S., Salles, J.F., Andreote, F.D. & Dini‐Andreote, F. (2021) Soil microbial diversity affects the plant‐root colonization by arbuscular mycorrhizal fungi. Microbial Ecology, 82, 100–103.
Friedman, J., Higgins, L.M. & Gore, J. (2017) Community structure follows simple assembly rules in microbial microcosms. Nature Ecology & Evolution, 1, 109.
Ghoul, M. & Mitri, S. (2016) The ecology and evolution of microbial competition. Trends in Microbiology, 24, 833–845.
Gülay, A., Musovic, S., Albrechtsen, H.‐J., Al‐Soud, W.A., Sørensen, S.J. & Smets, B.F. (2016) Ecological patterns, diversity and core taxa of microbial communities in groundwater‐fed rapid gravity filters. ISME Journal, 10, 2209–2222.
Guo, X. & Boedicker, J.Q. (2016) The contribution of high‐order metabolic interactions to the global activity of a four‐species microbial community. PLoS Computational Biology, 12, e1005079.
Harder, C.B., Nyrop Albers, C., Rosendahl, S., Aamand, J., Ellegaard‐Jensen, L. & Ekelund, F. (2019) Successional trophic complexity and biogeographical structure of eukaryotic communities in waterworks' rapid sand filters. FEMS Microbiology Ecology, 95, 1–13.
Hardin, G. (1960) The competitive exclusion principle: an idea that took a century to be born has implications in ecology, economics, and genetics. Science (1979), 131, 1292–1297.
Hibbing, M.E., Fuqua, C., Parsek, M.R. & Peterson, S.B. (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nature Reviews Microbiology, 8, 15–25.
Hodgson, D.J., Rainey, P.B. & Buckling, A. (2002) Mechanisms linking diversity, productivity and invasibility in experimental bacterial communities. Proceedings of the Royal Society of London, Series B: Biological Sciences, 269, 2277–2283.
Horemans, B., Raes, B., Vandermaesen, J., Simanjuntak, Y., Brocatus, H., T'Syen, J. et al. (2017) Biocarriers improve bioaugmentation efficiency of a rapid sand filter for the treatment of 2,6‐dichlorobenzamide‐contaminated drinking water. Environmental Science & Technology, 51, 1616–1625.
Horemans, B., Vandermaesen, J., Sekhar, A., Rombouts, C., Hofkens, J., Vanhaecke, L. et al. (2017) Aminobacter sp. MSH1 invades sand filter community biofilms while retaining 2,6‐dichlorobenzamide degradation functionality under C and N limiting conditions. FEMS Microbiology Ecology, 93, 1–10.
Ives, A.R. & Carpenter, S.R. (2007) Stability and diversity of ecosystems. Science (1979), 317, 58–62.
Jensen, A.L. (1987) Simple models for exploitative and interference competition. Ecological Modelling, 35, 113–121.
Johnsen, A.R., Hybholt, T.K., Jacobsen, O.S. & Aamand, J. (2009) A radiorespirometric method for measuring mineralization of [14C]‐compounds in a 96‐well microplate format. Journal of Microbiological Methods, 79, 114–116.
Jousset, A., Schulz, W., Scheu, S. & Eisenhauer, N. (2011) Intraspecific genotypic richness and relatedness predict the invasibility of microbial communities. ISME Journal, 5, 1108–1114.
Kaminsky, L.M., Trexler, R.V., Malik, R.J., Hockett, K.L. & Bell, T.H. (2019) The inherent conflicts in developing soil microbial inoculants. Trends in Biotechnology, 37, 140–151.
Katsuyama, C., Nakaoka, S., Takeuchi, Y., Tago, K., Hayatsu, M. & Kato, K. (2009) Complementary cooperation between two syntrophic bacteria in pesticide degradation. Journal of Theoretical Biology, 256, 644–654.
Kerr, B., Riley, M.A., Feldman, M.W. & Bohannan, B.J.M. (2002) Local dispersal promotes biodiversity in a real‐life game of rock–paper–scissors. Nature, 418, 171–174.
Kerr, M. & Churchill, G. (2001) Statistical design and the analysis of gene expression microarray data. Genetecis Research, 77, 123–128.
Kinnunen, M., Dechesne, A., Proctor, C., Hammes, F., Johnson, D., Quintela‐Baluja, M. et al. (2016) A conceptual framework for invasion in microbial communities. ISME Journal, 12, 2773–2779.
Lechón‐Alonso, P., Clegg, T., Cook, J., Smith, T.P. & Pawar, S. (2021) The role of competition versus cooperation in microbial community coalescence. PLoS Computational Biology, 17, e1009584.
Li, M., Wei, Z., Wang, J., Jousset, A., Friman, V.P., Xu, Y. et al. (2019) Facilitation promotes invasions in plant‐associated microbial communities. Ecology Letters, 22, 149–158.
Little, A.E.F., Robinson, C.J., Peterson, S.B., Raffa, K.F. & Handelsman, J. (2008) Rules of engagement: interspecies interactions that regulate microbial communities. Annual Review of Microbiology, 62, 375–401.
Liu, Z., Ma, A., Mathé, E., Merling, M., Ma, Q. & Liu, B. (2021) Network analyses in microbiome based on high‐throughput multi‐omics data. Briefings in Bioinformatics, 22, 1639–1655.
Mallon, C., Poly, F., Le Roux, X., Marring, I., Van Elsas, J. & Salles, J. (2015) Resource pulses can alleviate the biodiversity‐invasion relationship in soil microbial communities. Ecology, 96, 915–926.
Mallon, C., Van Elsas, J. & Salles, J. (2015) Microbial invasions: the process, patterns, and mechanisms. Trends in Microbiology, 23, 719–729.
Mallon, C.A., Le Roux, X., Van Doorn, G.S., Dini‐Andreote, F., Poly, F. & Salles, J.F. (2018) The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader's niche. ISME Journal, 12, 728–741.
Mauger, S., Monard, C., Thion, C. & Vandenkoornhuyse, P. (2022) Contribution of single‐cell omics to microbial ecology. Trends in Ecology & Evolution, 37, 67–78.
Mawarda, P.C., Lakke, S.L., Dirk van Elsas, J. & Salles, J.F. (2022) Temporal dynamics of the soil bacterial community following Bacillus invasion. iScience, 25, 1–17.
Mawarda, P.C., Le Roux, X., Acosta, M.U., van Elsas, J.D. & Salles, J.F. (2022) The impact of protozoa addition on the survivability of Bacillus inoculants and soil microbiome dynamics. ISME Communications, 2, 82.
Mawarda, P.C., Le Roux, X., van Elsas, J.D. & Salles, J.F. (2020) Deliberate introduction of invisible invaders: a critical appraisal of the impact of microbial inoculants on soil microbial communities. Soil Biology and Biochemistry, 148, 107874.
Mawarda, P.C., Mallon, C.A., Le Roux, X., van Elsas, J.D. & Salles, J.F. (2022) Interactions between bacterial inoculants and native soil bacterial community: the case of spore‐forming Bacillus spp. FEMS Microbiology Ecology, 98, 1–11.
Mayfield, M.M. & Stouffer, D.B. (2017) Higher‐order interactions capture unexplained complexity in diverse communities. Nature Ecology & Evolution, 1, 1–7.
Momeni, B., Xie, L. & Shou, W. (2017) Lotka‐Volterra pairwise modeling fails to capture diverse pairwise microbial interactions. eLife, 6, e25051.
Moons, P., Michiels, C.W. & Aertsen, A. (2009) Bacterial interactions in biofilms. Critical Reviews in Microbiology, 35, 157–168.
Morris, B.E.L., Henneberger, R., Huber, H. & Moissl‐Eichinger, C. (2013) Microbial syntrophy: interaction for the common good. FEMS Microbiology Review, 37, 384–406.
Nadell, C.D., Drescher, K., Wingreen, N.S. & Bassler, B.L. (2015) Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME Journal, 9, 1700–1709.
Sekhar, A., Horemans, B., Aamand, J., Sørensen, S.R., Vanhaecke, L., Bussche, J.V. et al. (2016) Surface colonization and activity of the 2,6‐Dichlorobenzamide (BAM) degrading Aminobacter sp. strain MSH1 at macro‐ and micropollutant BAM concentrations. Environmental Science & Technology, 50, 10123–10133.
Shade, A., Peter, H., Allison, S.D., Baho, D.L., Berga, M., Bürgmann, H. et al. (2012) Fundamentals of microbial community resistance and resilience. Frontiers in Microbiology, 3, 417.
Shasha, D.E., Kouranov, A.Y., Lejay, L.V., Chou, M.F. & Coruzzi, G.M. (2001) Using combinatorial design to study regulation by multiple input signals. A tool for parsimony in the post‐genomics era. Plant Physiology, 127, 1590–1594.
Stachowicz, J.J. & Tilman, D. (2005) Species invasions and the relationships between species diversity, community saturation, and ecosystem functioning. In: Sax, D.F., Stachowicz, J.J. & Gaines, D.D. (Eds.) Species invasions: insights into ecology, evolution, and biogeography. Sunderland, MA: Sinauer Associates, pp. 41–64.
Tilman, D. (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proceedings of the National Academy of Sciences, 101, 10854–10861.
Van Elsas, J., Chiurazzi, M., Mallon, C., Elhottova, D., Krištůfek, V. & Salles, J. (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. Proceedings of the National Academy of Sciences, 109, 1159–1164.
Van Nevel, S., De Roy, K. & Boon, N. (2013) Bacterial invasion potential in water is determined by nutrient availability and the indigenous community. FEMS Microbiology Ecology, 85, 593–603.
Vandermaesen, J., Du, S., Daly, A.J., Baetens, J.M., Horemans, B., De Baets, B. et al. (2022) Interspecies interactions of the 2,6‐dichlorobenzamide degrading Aminobacter sp. MSH1 with resident sand filter bacteria: indications for mutual cooperative interactions that improve BAM mineralization activity. Environmental Science & Technology, 56, 1352–1364.
Vandermaesen, J., Lievens, B. & Springael, D. (2017) Isolation and identification of culturable bacteria, capable of heterotrophic growth, from rapid sand filters of drinking water treatment plants. Research in Microbiology, 168, 594–607.
Venturelli, O.S., Carr, A.V., Fisher, G., Hsu, R.H., Lau, R., Bowen, B.P. et al. (2018) Deciphering microbial interactions in synthetic human gut microbiome communities. Molecular Systems Biology, 14, e8157.
Vivant, A.L., Garmyn, D., Maron, P.A., Nowak, V. & Piveteau, P. (2013) Microbial diversity and structure are drivers of the biological barrier effect against Listeria monocytogenes in soil. PLoS One, 8, e76691.
Wei, Z., Yang, T., Friman, V.P., Xu, Y., Shen, Q. & Jousset, A. (2015) Trophic network architecture of root‐associated bacterial communities determines pathogen invasion and plant health. Nature Communications, 6, 8413.
West, S.A. & Cooper, G.A. (2016) Division of labour in microorganisms: an evolutionary perspective. Nature Reviews. Microbiology, 14, 716–723.
Whiley, R.A., Fleming, E.V., Makhija, R. & Waite, R.D. (2015) Environment and colonisation sequence are key parameters driving cooperation and competition between Pseudomonas aeruginosa cystic fibrosis strains and oral commensal streptococci. PLoS One, 10, e0115513.
Wu, Y., Fu, C., Peacock, C.L., Sørensen, S.J., Redmile‐Gordon, M.A., Xiao, K.‐Q. et al. (2023) Cooperative microbial interactions drive spatial segregation in porous environments. Nature Communications, 14, 4226.
Xu, X., Zarecki, R., Medina, S., Ofaim, S., Liu, X., Chen, C. et al. (2019) Modeling microbial communities from atrazine contaminated soils promotes the development of biostimulation solutions. ISME Journal, 13, 494–508.
Yang, T., Wei, Z., Friman, V.P., Xu, Y., Shen, Q., Kowalchuk, G.A. et al. (2017) Resource availability modulates biodiversity‐invasion relationships by altering competitive interactions. Environmental Microbiology, 19, 2984–2991.