Butterflies in the gut: the interplay between intestinal microbiota and stress

Lai, Tzu-Ting; Liou, Chia-Wei; Tsai, Yu-Hsuan; Lin, Yuan-Yuan; Wu, Wei-Li

doi:10.1186/s12929-023-00984-6

Journal of Biomedical Science

Table 1 Adaptation of commensal microbiome and behavior under acute and chronic stress conditions

From: Butterflies in the gut: the interplay between intestinal microbiota and stress

Stress model	Stress period	Strain	Age	Sex	Vendor	Food	Sample	Trend	Rank	Identified bacteria	Phylum	Fold change	Behavior test	Behavior test outcome	Reference (PMID)
UCMS	8w	C57BL/6J	16w	Male	Janvier laboratory	N/A	Feces	Decrease	f	Lactobacillaceae	Firmicutes	N/A	Novelty suppressed feeding test	Increased time of latency to eat	33311466
													Splash test	Increased time of latency to groom
													Tail suspension test	Increased time of immobility
													Forced swimming test	Increased time of immobility
													Light/dark box test	No change
UCMS	5w	C57BL/6J	14w	Male	Jackson laboratory	N/A	Feces	Increase	g	Cyanobacterium	Cyanobacteria	3803.0271	Forced swimming test	Decreased time of escape behavior	28266612
									g	Allobaculum	Firmicutes	515.0243	Open-field test	No change
									g	Bifidobacterium	Actinobacteria	70.4967
									g	Anaerofustis	Firmicutes	8.4009
									g	Clostridium	Firmicutes	7.2681
									g	Ruminococcus	Firmicutes	6.1411
									f	Lachnospiraceae	Firmicutes	2.9609
									f	Erysipelotrichaceae	Firmicutes	2.2803
								Decrease	g	Lactobacillus	Firmicutes	7.9232
									g	Anaeroplasma	Tenericutes	7.1972
									f	Turicibacteraceae	Firmicutes	5.6748
									g	Coprococcus	Firmicutes	3.8667
									c	Mollicutes	Tenericutes	3.5037
									f	Peptococcaceae	Firmicutes	2.9847
									g	Eubacterium	Firmicutes	2.7191
									o	Clostridiales	Firmicutes	1.8332
									f	Catabacteriaceae	Firmicutes	1.8304
UCMS	8w	C57BL/6J	16w	Male	Janvier laboratory	N/A	Feces	Decrease	p	Firmicutes	Firmicutes	N/A	Tail suspension test	Increased time of immobility	32187541
									p	Tenericutes	Tenericutes	N/A	Forced swimming test	Increased time of immobility
									p	Saccharibacteria	Saccharibacteria	N/A
CSDS	5m/d, 1w	C57BL/6J	9w	Male	Jackson laboratory	Prolab® RMH 3500	Feces	Increase	p	Mucispirillum	Mucispirillum	326.3333	Open-field test	Decreased the travel distance	30824791
						LabDiet, St. Louis, MO			g	Candidatus Arthromitus	Firmicutes	181.0000	Open-field test	Decreased time spent in center zone
									g	Bilophila	Proteobacteria	24.5000	Sucrose preference test	Decreased sucrose preference
									g	Helicobacter	Proteobacteria	11.8182	Forced swimming test	Increased time of immobility
									g	Flexispira	Proteobacteria	9.7307
									g	Odoribacter	Bacteroidetes	7.9181
									g	Dehalobacterium	Firmicutes	1.8105
									g	Coprococcus	Firmicutes	1.7233
									g	Ruminococcus	Firmicutes	1.6582
									g	Oscillospira	Firmicutes	1.6153
								Decrease	g	Turicibacter	Firmicutes	26.3000
									g	Paraprevotella	Bacteroidetes	16.0202
									g	Allobaculum	Firmicutes	9.0435
									g	Bifidobacterium	Actinobacteria	8.6522
									g	Akkermansia	Verrucomicrobiota	4.0375
									f	Mogibacteriaceae	Firmicutes	2.6246
									f	Nitrosomonadaceae	Proteobacteria	2.5000
									f	Coriobacteriaceae	Actinobacteria	2.3158
									g	Anaerostipes	Firmicutes	2.1546
									g	Dorea	Firmicutes	2.1289
CSDS	5m/d, 10d	C57BL/6J	8–9w	Male	National Laboratory Animal Center	N/A	Feces	Increase	f	Bacteroidales S24–7	Bacteroidetes	N/A	Social interaction test	Decreased the social index	34327733
					NLAC, Taipei, Taiwan				f	Porphyromonadaceae	Bacteroidetes	N/A	Open-field test	Decreased the travel distance
									g	Bacteroides	Bacteroidetes	N/A	Open-field test	Decreased time spent in center zone
								Decrease	g	Enterorhabdus	Actinobacteria	N/A	Sucrose preference test	Decreased sucrose preference
									f	Unclassified Bacteroidales S24-7	Bacteroidetes	N/A
									f	Ruminococcaceae	Firmicutes	N/A
CSDS	5m/d, 10d	C57BL/6J	12–13w	Male	Charles River Japan	CE-2, CLEA Japan	Feces	Increase	p	Bacteroidetes	Bacteroidetes	N/A	Social interaction test	Decreased the social time	33972646
						Tokyo, Japan			p	Actinobacteria	Actinobacteria	N/A		Decreased distance traveled
									p	Proteobacteria	Proteobacteria	N/A
								Decrease	p	Firmicutes	Firmicutes	N/A
SOC	10 mice/cage, 19w	C57BL/6J	23w	Male	Jackson laboratory	N/A	Feces	Increase	g	Allobaculum	Firmicutes	LDA score	Open-field test	No difference	34856844
									f	Verrucomicrobiaceae	Verrucomicrobia	(high to low)	Elevated plus maze	Increased of the speed
									c	Verrucomicrobiae	Verrucomicrobia		Light/dark box test	Increased number of entries in the dark
									p	Verrucomicrobia	Verrucomicrobia
									s	muciniphila	Verrucomicrobia
									g	Akkermansia	Verrucomicrobia
									o	Turicibacteraies	Firmicutes
									g	Turicibacter	Firmicutes
									f	Planococcaceae	Firmicutes
									g	Anaerostipes	Firmicutes	N/A
								Decrease	g	Bacteroides	Bacteroidetes	LDA score
									f	Bacteroidaceae	Bacteroidetes	(high to low)
									f	Lactobacilliaceae	Firmicutes
									g	Lactobacillus	Firmicutes
									f	Paraprevotellaceae	Bacteroidetes
									g	Prevotella	Bacteroidetes
									f	Clostridiaceae	Firmicutes
									g	Ruminnococcus	Firmicutes
									s	Ruminnococcus gnavus	Firmicutes
									f	Hellicobacteraceae	Proteobacteria
									s	Bacteroides acidifaciens	Bacteroidetes	N/A
									f	Erysipelotrichaceae	Firmicutes	N/A
CSDS + SOC	3w	C57BL/6J	18w	Male	Harlan, UK	N/A	Cecal content	Increase	f	Helicobacteracea	Proteobacteria	N/A	Social interaction test	Decreased social interaction ratio	30066368
	SOC = 10 mice/cage, 24 h								g	Prevotellaceae UCG 001	Bacteroidetes	N/A	Three chamber test	No change
	CSDS = 2 h/d								f	Prevotellaceae	Bacteroidetes	N/A	Open-field test	No change
									o	Gastranaerophilales	Melainabacteria	N/A	Forced swimming test	No change
								Decrease	g	Ruminicoccaceae UCG 013	Firmicutes	N/A	Female urine sniffing test	Decreased interaction time
									g	Intestinimonas	Firmicutes	N/A	Marble burying test	No change
													Elevated plus maze	No change
													Tail suspension test	No change
													Sucrose preference test	Increased sucrose preference
													Novel object recognition test	No change
													Hot plate test	No change
RS	2 h/d, 5times/w, 6w	C57BL/6J	17-19w	Male	Harlan	N/A	Feces	Increase	f	Lachnospiraceae	Firmicutes	2.0900	Rotarod performance	No change	30579705
								Decrease	g	Lactobacillus	Firmicutes	2.9700
RS	2 h/d, 7d	C57BL/6J	7-11w	Both	Jackson laboratory	Lab Diet 5053	Feces	Increase	f	Bacteroidaceae	Bacteroidetes	N/A	N/A	N/A	33196055
									o	Unclassical Burkholderiales	Proteobacteria	N/A
								Decrease	f	Ruminococcaceae	Firmicutes	N/A
									f	Coriobacteriaceae	Actinobacteria	N/A
									f	Unclassical Clostridiales	Firmicutes	N/A
RS	2 h/d, 10d	C57BL/6J	7-8w	Male	Orient Animal Breeding Center	N/A	Feces	Increase	p	Proteobacteria	Proteobacteria	N/A	Elevated plus maze	Decreased time spent in open arms	30224732
					(Seoul, Korea)				f	Helicobacteraceae	Proteobacteria	N/A	Light/dark box test	Decreased time spent in light area
									f	Enterobacteriaceae	Proteobacteria	N/A	Marble-burying test	Increased percentage of marble buried
									g	Klebsiella	Proteobacteria	N/A
									g	Helicobacter	Proteobacteria	N/A
								Decrease	p	Actinobacteria	Actinobacteria	N/A
									p	Bacteroidetes	Bacteroidetes	N/A
									f	Lactobacillaceae	Firmicutes	N/A
RS	4–6 h/d, 21d	C57BL/6J	12-16w	Male	Australian Phenomics	N/A	Feces	Increase	f	Lachnospiraceae	Firmicutes	1.0030	Forced swimming test	Increased floating time	27090302
								Decrease	g	Allobaculum	Firmicutes	1.0840	Elevated plus maze	Decreased time into open arm
									g	Bifidobacterium	Actinobacteria	1.0480
									g	Turicibacter	Firmicutes	1.0350
									g	Clostridium	Firmicutes	1.0070
RS	16 h/d, 1d	C57BL/6N	6-8w	Male	Charles River Laboratories	N/A	Ileum	Increase	g	Escherichia_Shigella	Proteobacteria	LDA score	N/A	N/A	34795263
									f	Enterobacteriaceae	Proteobacteria	(high to low)
									o	Enterobacteriales	Proteobacteria
									p	Proteobacteria	Proteobacteria
									c	Gammaproteobacteria	Proteobacteria
									g	Enterococcus	Firmicutes
									f	Enterococcaceae	Firmicutes
									g	Staphylococcus	Firmicutes
									g	Streptococcus	Firmicutes
									f	Streptococcaceae	Firmicutes
								Decrease	p	Firmicutes	Firmicutes	LDA score
									c	Erysipelotrichia	Firmicutes	(high to low)
									f	Erysipelotrichaceae	Firmicutes
									o	Erysipelotrichales	Firmicutes
									g	lleibacterium	Firmicutes
									f	Muribaculaceae	Bacteroidetes
									c	Bacteroidia	Bacteroidetes
									o	Bacteroidales	Bacteroidetes
									p	Bacteroidetes	Bacteroidetes
									p	Actinobacteria	Actinobacteria
							Cecum	Increase	f	Enterobacteriaceae	Proteobacteria	LDA score
									o	Enterobacteriales	Proteobacteria	(high to low)
									c	Gammaproteobacteria	Proteobacteria
									p	Proteobacteria	Proteobacteria
									g	Mucispirillum	Deferribacteres
									p	Deferribacteres	Deferribacteres
									f	Deferribacteraceae	Deferribacteres
									o	Deferribacterales	Deferribacteres
									g	Escherichia-Shigella	Proteobacteria
								Decrease	c	Clostridia	Firmicutes	LDA score
									o	Clostridiales	Firmicutes	(high to low)
									f	Lachnospiraceae	Firmicutes
									g	Lachnospiraceae_NK4A136_group	Firmicutes
									f	Muribaculaceae	Bacteroidetes
									f	Erysipelotrichaceae	Firmicutes
									o	Erysipelotrichales	Firmicutes
									c	Erysipelotrichia	Firmicutes
									g	lleibacterium	Firmicutes
									g	Clostridiales_vadinBB60_group	Firmicutes
							Colon	Increase	g	Bacteroides	Bacteroidetes	LDA score
									f	Bacteroidaceae	Bacteroidetes	(high to low)
									f	Enterobacteriaceae	Proteobacteria
									o	Enterobacteriales	Proteobacteria
									g	Escherichia_Shigella	Proteobacteria
									g	Gammaproteobacteria	Proteobacteria
									p	Proteobacteria	Proteobacteria
									f	Deferribacteraceae	Deferribacteres
									p	Deferribacteres	Deferribacteres
									o	Deferribacterales	Deferribacteres
								Decrease	p	Firmicutes	Firmicutes	LDA score
									o	Erysipelotrichales	Firmicutes	(high to low)
									f	Erysipelotrichaceae	Firmicutes
									c	Erysipelotrichia	Firmicutes
									g	lleibacterium	Firmicutes
									g	Lachnospiraceae_NK4A136_group	Firmicutes
									f	Lactobacillaceae	Firmicutes
									g	Lactobacillus	Firmicutes
									o	Rhodospirillales/NA/NA	Proteobacteria
									c	Alphaproteobacteria	Proteobacteria
RS	3–4 h/d, 14d	C57BL/6J	13w	Male	Nanjing Medical University	N/A	Feces	Increase	g	Akkermansia	Verrucomicrobia	N/A	Forced swimming test	Increased immobility time	33535879
									g	Anaerofustis	Firmicutes	N/A	Sucrose preference test	Decreased sucrose preference
								Decrease	g	Parabacteroides	Bacteroidetes	N/A	Elevated plus maze	Decreased duration in open arms
									f	Lachnospiraceae	Firmicutes	N/A	Open-field test	Decreased center time
									g	Ruminococcus	Firmicutes	N/A
									f	Unclassified_Ruminococcaceae	Firmicutes	N/A
WAS	1 h/d, 10 d	C57BL/6J	6-7w	Female	Charles River Laboratories	N/A	Feces	Increase	c	Gammaproteobacteria	Proteobacteria	3.0000	N/A	N/A	23470617
									p	Firmicutes	Firmicutes	2.0000
								Decrease	p	Bacteroidetes	Bacteroidetes	2.0000
							Small intestine	Increase	o	unclassified Clostridiales	Firmicutes	N/A
							content		f	Clostridiaceae	Firmicutes	N/A
									f	Streptococcaceae	Firmicutes	N/A
								Decrease	f	Lactobacillaceae	Firmicutes	N/A
									f	Lachnospiraceae	Firmicutes	N/A
									p	Unclassified Bacteroidetes	Bacteroidetes	N/A
									f	Ruminococcaceae	Firmicutes	N/A
									p	unclassified Firmicutes	Firmicutes	N/A
							Colon mucosa	Decrease	f	Porphyromonadaceae	Bacteroidetes	N/A
									p	unclassified Bacteroidetes	Bacteroidetes	N/A
							Colon content	Decrease	f	Lactobacillaceae	Firmicutes	N/A
WAS	1 h/d, 10d	C57BL/6J	7–8w	Female	Charles River Laboratories	N/A	Feces	No change		No change	N/A	No change	Light/dark box test	No change	20966022
WAS	1 h/d, 1d	C57BL/6J	6–8w	Both	Jackson laboratory	N/A	N/A	N/A		N/A		N/A	Novel object recognition test	No change	31652348
													Light/dark box test	No change
													Open-field test	Decreased the travel distance

UCMS = unpredictable chronic mild stress, p = Phylum, CSDS = chronic social defeat stress, c = Class, RS = restraint stress, o = Order, WAS = water avoidance stress, f = Family, SOC: social overcrowding, g = genus, N/A: not applicable, s = species

Back to article page

ISSN: 1423-0127

Contact us

Submission enquiries: Access here and click Contact Us
General enquiries: info@biomedcentral.com