Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat

被引:32
作者
Wein, Tanita [1 ]
Dagan, Tal [1 ]
Fraune, Sebastian [2 ]
Bosch, Thomas C. G. [2 ]
Reusch, Thorsten B. H. [3 ]
Huelter, Nils F. [1 ]
机构
[1] Christian Albrechts Univ Kiel, Inst Microbiol, Kiel, Germany
[2] Christian Albrechts Univ Kiel, Inst Zool, Kiel, Germany
[3] GEOMAR Helmholtz Ctr Ocean Res Kiel, Kiel, Germany
来源
FRONTIERS IN MICROBIOLOGY | 2018年 / 9卷
基金
欧洲研究理事会;
关键词
Curvibacter; microbial ecology; host-microbe interactions; metaorganisms; Hydra; VIBRIO-FISCHERI; MICROBIOTA; COMPETITION; ECOLOGY; PROTEIN; SQUID; MODEL;
D O I
10.3389/fmicb.2018.00443
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
Most eukaryotic species are colonized by a microbial community - the microbiota that is acquired during early life stages and is critical to host development and health. Much research has focused on the microbiota biodiversity during the host life, however, empirical data on the basic ecological principles that govern microbiota assembly is lacking. Here we quantify the contribution of colonizer order, arrival time and colonization history to microbiota assembly on a host. We established the freshwater polyp Hydra vulgaris and its dominant colonizer Curvibacter as a model system that enables the visualization and quantification of colonizer population size at the single cell resolution, in vivo, in real time. We estimate the carrying capacity of a single Hydra polyp as 2 x 10(5) Curvibacter cells, which is robust among individuals and time. Colonization experiments reveal a clear priority effect of first colonizers that depends on arrival time and colonization history. First arriving colonizers achieve a numerical advantage over secondary colonizers within a short time lag of 24 h. Furthermore, colonizers primed for the Hydra habitat achieve a numerical advantage in the absence of a time lag. These results follow the theoretical expectations for any bacterial habitat with a finite carrying capacity. Thus, Hydra colonization and succession processes are largely determined by the habitat occupancy over time and Curvibacter colonization history. Our experiments provide empirical data on the basic steps of host-associated microbiota establishment the colonization stage. The presented approach supplies a framework for studying habitat characteristics and colonization dynamics within the host-microbe setting.
引用
收藏
页数:10
相关论文
共 41 条
[1]   Plasticity of epithelial cell shape in response to upstream signals: A whole-organism study using transgenic Hydra [J].
Anton-Erxleben, Friederike ;
Thomas, Antje ;
Wittlieb, Joerg ;
Fraune, Sebastian ;
Bosch, Thomas C. G. .
ZOOLOGY, 2009, 112 (03) :185-194
[2]   A secreted antibacterial neuropeptide shapes the microbiome of Hydra [J].
Augustin, Rene ;
Schroeder, Katja ;
Rincon, Andrea P. Murillo ;
Fraune, Sebastian ;
Anton-Erxleben, Friederike ;
Herbst, Eva-Maria ;
Wittlieb, Joerg ;
Schwentner, Martin ;
Groetzinger, Joachim ;
Wassenaar, Trudy M. ;
Bosch, Thomas C. G. .
NATURE COMMUNICATIONS, 2017, 8
[3]   Microbiomes: unifying animal and plant systems through the lens of community ecology theory [J].
Christian, Natalie ;
Whitaker, Briana K. ;
Clay, Keith .
FRONTIERS IN MICROBIOLOGY, 2015, 6
[4]   The Application of Ecological Theory Toward an Understanding of the Human Microbiome [J].
Costello, Elizabeth K. ;
Stagaman, Keaton ;
Dethlefsen, Les ;
Bohannan, Brendan J. M. ;
Relman, David A. .
SCIENCE, 2012, 336 (6086) :1255-1262
[5]   The ecology of the microbiome: Networks, competition, and stability [J].
Coyte, Katharine Z. ;
Schluter, Jonas ;
Foster, Kevin R. .
SCIENCE, 2015, 350 (6261) :663-666
[6]   Chromosomal Complementation Using Tn7 Transposon Vectors in Enterobacteriaceae [J].
Crepin, Sebastien ;
Harel, Jos ;
Dozois, Charles M. .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2012, 78 (17) :6001-6008
[7]   Microbial interactions lead to rapid micro-scale successions on model marine particles [J].
Datta, Manoshi S. ;
Sliwerska, Elzbieta ;
Gore, Jeff ;
Polz, Martin F. ;
Cordero, Otto X. .
NATURE COMMUNICATIONS, 2016, 7
[8]   Evolving Perspectives on Monopolization and Priority Effects [J].
De Meester, Luc ;
Vanoverbeke, Joost ;
Kilsdonk, Laurens J. ;
Urban, Mark C. .
TRENDS IN ECOLOGY & EVOLUTION, 2016, 31 (02) :136-146
[9]   First arrived takes all: inhibitory priority effects dominate competition between co-infecting Borrelia burgdorferi strains [J].
Devevey, Godefroy ;
Dang, Trang ;
Graves, Christopher J. ;
Murray, Sarah ;
Brisson, Dustin .
BMC MICROBIOLOGY, 2015, 15
[10]  
Douglas AE, 2016, MBIO, V7, DOI [10.1128/mBio.02099, 10.1128/mBio.02099-15]