Cooperative microbial interactions drive spatial segregation in porous environments.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
15 07 2023
Historique:
received: 26 05 2022
accepted: 05 07 2023
medline: 17 7 2023
pubmed: 16 7 2023
entrez: 15 7 2023
Statut: epublish

Résumé

The role of microbial interactions and the underlying mechanisms that shape complex biofilm communities are poorly understood. Here we employ a microfluidic chip to represent porous subsurface environments and show that cooperative microbial interactions between free-living and biofilm-forming bacteria trigger active spatial segregation to promote their respective dominance in segregated microhabitats. During initial colonization, free-living and biofilm-forming microbes are segregated from the mixed planktonic inoculum to occupy the ambient fluid and grain surface. Contrary to spatial exclusion through competition, the active spatial segregation is induced by cooperative interactions which improves the fitness of both biofilm and planktonic populations. We further show that free-living Arthrobacter induces the surface colonization by scavenging the biofilm inhibitor, D-amino acids and receives benefits from the public goods secreted by the biofilm-forming strains. Collectively, our results reveal how cooperative microbial interactions may contribute to microbial coexistence in segregated microhabitats and drive subsurface biofilm community succession.

Identifiants

pubmed: 37454222
doi: 10.1038/s41467-023-39991-4
pii: 10.1038/s41467-023-39991-4
pmc: PMC10349867
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4226

Informations de copyright

© 2023. The Author(s).

Références

Appl Environ Microbiol. 2019 Jul 1;85(14):
pubmed: 31076430
ISME J. 2019 Jul;13(7):1700-1710
pubmed: 30833685
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Commun. 2020 Sep 18;11(1):4717
pubmed: 32948774
Nat Commun. 2020 May 15;11(1):2418
pubmed: 32415107
Cold Spring Harb Protoc. 2010 Jun;2010(6):pdb.prot5439
pubmed: 20516177
J Comput Biol. 2012 May;19(5):455-77
pubmed: 22506599
Mol Biol Evol. 2014 Jan;31(1):232-8
pubmed: 24170494
Nat Commun. 2016 Jun 17;7:11965
pubmed: 27311813
Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
J Chromatogr A. 2014 Jan 10;1324:109-14
pubmed: 24315356
Arch Microbiol. 1981 Jul;129(5):395-400
pubmed: 7283636
Science. 2010 Apr 30;328(5978):627-9
pubmed: 20431016
Soil Biol Biochem. 2018 Aug;123:115-125
pubmed: 31579317
NPJ Biofilms Microbiomes. 2021 Jan 27;7(1):10
pubmed: 33504794
Nat Biotechnol. 2012 Oct;30(10):918-20
pubmed: 23051804
Environ Microbiol. 2022 Oct;24(10):4755-4770
pubmed: 35837862
Innovation (Camb). 2021 Jul 01;2(3):100141
pubmed: 34557778
BMC Res Notes. 2016 Feb 12;9:88
pubmed: 26868221
Environ Sci Technol. 2020 Jun 2;54(11):6919-6928
pubmed: 32348125
Environ Microbiol. 2006 May;8(5):871-84
pubmed: 16623744
Nature. 2003 Sep 4;425(6953):72-4
pubmed: 12955142
Proc Natl Acad Sci U S A. 2017 Jan 10;114(2):E161-E170
pubmed: 28007984
Appl Environ Microbiol. 2018 Nov 30;84(24):
pubmed: 30291118
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Nat Methods. 2016 Jul;13(7):581-3
pubmed: 27214047
ISME J. 2022 Jun;16(6):1512-1522
pubmed: 35121821
Appl Environ Microbiol. 2009 Dec;75(23):7537-41
pubmed: 19801464
ISME J. 2018 Jun;12(6):1582-1593
pubmed: 29563570
Bioinformatics. 2010 Jun 1;26(11):1463-4
pubmed: 20395285
Appl Microbiol Biotechnol. 2015 Apr;99(8):3519-32
pubmed: 25786738
ISME J. 2021 Oct;15(10):3019-3033
pubmed: 33953363
Appl Environ Microbiol. 2015 Dec;81(24):8414-26
pubmed: 26431965
Ecol Lett. 2009 Sep;12(9):949-60
pubmed: 19702749
Bioinformatics. 2010 Oct 1;26(19):2460-1
pubmed: 20709691
Appl Environ Microbiol. 2016 Jun 30;82(14):4401-4409
pubmed: 27208104
Nat Rev Microbiol. 2004 Feb;2(2):95-108
pubmed: 15040259
Nucleic Acids Res. 2012 Aug;40(15):e115
pubmed: 22730293
J Bacteriol. 2013 Dec;195(23):5391-5
pubmed: 24097941
Proc Natl Acad Sci U S A. 2008 Nov 25;105(47):18188-93
pubmed: 19011107
Nat Commun. 2018 Jan 2;9(1):19
pubmed: 29296020
Appl Environ Microbiol. 2017 Dec 15;84(1):
pubmed: 29079618
Elife. 2017 Jan 13;6:
pubmed: 28084994
Appl Environ Microbiol. 2013 Feb;79(4):1396-9
pubmed: 23220960
Lab Chip. 2008 Dec;8(12):2151-6
pubmed: 19023479
Nat Microbiol. 2021 Feb;6(2):196-208
pubmed: 33398099
Nat Commun. 2018 Jul 16;9(1):2743
pubmed: 30013041
Anal Biochem. 1987 Jan;160(1):47-56
pubmed: 2952030
J Am Soc Mass Spectrom. 1994 Sep;5(9):859-66
pubmed: 24222034
Curr Opin Microbiol. 2016 Jun;31:227-234
pubmed: 27232202
Nat Commun. 2020 Mar 18;11(1):1440
pubmed: 32188849
Environ Microbiol. 2016 Sep;18(8):2565-74
pubmed: 27119650
Front Microbiol. 2018 Apr 06;9:683
pubmed: 29681896
PLoS One. 2010 Mar 10;5(3):e9490
pubmed: 20224823
Nat Commun. 2017 May 31;8:15416
pubmed: 28561030
Proc Natl Acad Sci U S A. 2017 Oct 3;114(40):10666-10671
pubmed: 28923953
mSystems. 2021 May 11;6(3):
pubmed: 33975969
Environ Int. 2019 Nov;132:105116
pubmed: 31479959
J Mass Spectrom. 2010 Jul;45(7):703-14
pubmed: 20623627
Arch Microbiol. 2018 Dec;200(10):1419-1425
pubmed: 30039322
Nat Rev Microbiol. 2016 Sep;14(9):589-600
pubmed: 27452230
Nat Methods. 2010 May;7(5):335-6
pubmed: 20383131
Nat Rev Microbiol. 2019 Apr;17(4):247-260
pubmed: 30760902
Nucleic Acids Res. 2007 Jan;35(Database issue):D527-32
pubmed: 17098933
Environ Sci Technol. 2018 Nov 6;52(21):12265-12274
pubmed: 30257556
ISME J. 2021 Jan;15(1):29-40
pubmed: 32887945
Microbiol Mol Biol Rev. 2017 Oct 11;81(4):
pubmed: 29021219
Curr Biol. 2019 Nov 4;29(21):3622-3634.e5
pubmed: 31630946
Nat Ecol Evol. 2021 Feb;5(2):195-203
pubmed: 33398106
Nat Rev Microbiol. 2016 Apr;14(4):251-63
pubmed: 26972916
Bioinformatics. 2015 Feb 15;31(4):587-9
pubmed: 25338718
ISME J. 2022 Jan;16(1):296-306
pubmed: 34321619

Auteurs

Yichao Wu (Y)

State Key Laboratory of Agricultural Microbiology, College of Resources and Environment, Huazhong Agricultural University, Wuhan, China.

Chengxia Fu (C)

State Key Laboratory of Agricultural Microbiology, College of Resources and Environment, Huazhong Agricultural University, Wuhan, China.

Caroline L Peacock (CL)

School of Earth and Environment, University of Leeds, Leeds, LS2 9JT, UK.

Søren J Sørensen (SJ)

Section of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Marc A Redmile-Gordon (MA)

Department of Environmental Horticulture, Royal Horticultural Society, Wisley, Surrey, GU23 6QB, UK.

Ke-Qing Xiao (KQ)

School of Earth and Environment, University of Leeds, Leeds, LS2 9JT, UK.
State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, China.

Chunhui Gao (C)

State Key Laboratory of Agricultural Microbiology, College of Resources and Environment, Huazhong Agricultural University, Wuhan, China.

Jun Liu (J)

State Key Laboratory of Agricultural Microbiology, College of Resources and Environment, Huazhong Agricultural University, Wuhan, China.

Qiaoyun Huang (Q)

State Key Laboratory of Agricultural Microbiology, College of Resources and Environment, Huazhong Agricultural University, Wuhan, China.

Zixue Li (Z)

School of Physics, Huazhong University of Science and Technology, Wuhan, China.

Peiyi Song (P)

School of Physics, Huazhong University of Science and Technology, Wuhan, China.

Yongguan Zhu (Y)

State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, China.
Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China.

Jizhong Zhou (J)

Institute for Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, USA.
State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China.
Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, USA.
School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, USA.

Peng Cai (P)

State Key Laboratory of Agricultural Microbiology, College of Resources and Environment, Huazhong Agricultural University, Wuhan, China. cp@mail.hzau.edu.cn.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Aerosols Humans Decontamination Air Microbiology Masks
Coal Metagenome Phylogeny Bacteria Genome, Bacterial
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria

Classifications MeSH