Changes in Periodontal Health Status Are Associated with Bacterial Community Shifts as Assessed by Quantitative 16S Cloning and Sequencing

Purnima S. Kumar; Eugene J. Leys; Jennifer M. Bryk; Francisco J. Martinez; Melvin L. Moeschberger; Ann L. Griffen

doi:10.1128/JCM.00317-06

DOI: 10.1128/JCM.00317-06

Article Figures & Data

Figures

Tables
Additional Files

Open in new tab
Download powerpoint
FIG. 1.
Clinical stability of 24 subjects over 2 years. For the improved group, the shaded and open bars taken together indicate the number of sites with probe depths of >4 mm (deep sites) at baseline. Open bars represent decreases in the number of deep sites that occurred between the baseline and final sampling times. For the worse group, the shaded bars indicate initial clinical status and the solid bars represent increases in the number of deep sites that occurred between the baseline and final sampling times.
Open in new tab
Download powerpoint
FIG. 2.
Relationship between periodontal status and microbial stability and diversity for 24 subjects over 2 years. (Top) Relationship between clinical status and microbial conservation. (Center) Relationship between the number of species lost or gained over 2 years and clinical status. (Bottom) Relationship between mean microbial diversity (number of species present in each subject over 2 years) and clinical status. The standard deviation (small lines), group mean (central line in diamond), and 95% confidence intervals (height of diamond) are shown for each group.
Open in new tab
Download powerpoint
FIG. 3.
Mean levels at 2 years (top) and change in levels (mean level at 2 years minus mean level at baseline) (bottom) for species significantly associated with improvement or worsening of periodontitis. (Top) Percentage of total clones accounted for by each species for the stable healthy, improved, and worse groups at the final sampling time. (Bottom) Percentage of change between the initial and final sampling times for the same species and clinical groups. Species showing significant differences (P < 0.05) among the three clinical groups are indicated by an asterisk.

TABLE 1.

Species and phylotypes for each clinical group, arranged in order of decreasing frequency^a

Overall rank	Species/phylotype(s)	% of total clones^b	Mean % of total clones ± SD for individuals with the following clinical status:
Overall rank	Species/phylotype(s)	% of total clones^b	Stable	Better	Worse
1	Veillonella sp. oral clone X042	9.52	10.3 ± 4.0	8.1 ± 7.5	9.8 ± 8.1
2	Campylobacter gracilis	3.65	4.5 ± 4.3	4.2 ± 4.7	1.9 ± 2.6
3	Streptococcus mitis	3.48	3.4 ± 3.2	3.4 ± 3.2	3.5 ± 2.2
4	Streptococcus gordonii	3.21	4.5 ± 5.7	3.1 ± 1.8	1.5 ± 1.7
5	Streptococcus oralis	2.75	2.7 ± 2.3	3.4 ± 2.9	2.1 ± 1.9
6	Streptococcus sanguinis	2.42	3.2 ± 3.9	1.9 ± 2.4	1.9 ± 2.0
7	Streptococcus sp. oral strain 12F	2.42	2.7 ± 2.0	3.5 ± 3.9	1.0 ± 1.7
8	Peptostreptococcus sp. oral clone FG014	2.17	2.1 ± 2.1	2.3 ± 2.6	2.1 ± 5.1
9	Selenomonas infelix	2.13	2.0 ± 1.9	1.8 ± 1.4	2.7 ± 2.4
10	Campylobacter showae	1.92	1.9 ± 2.1	2.0 ± 2.9	1.9 ± 2.8
11	Peptostreptococcus sp. oral clone AJ062	1.90	0.9 ± 2.3	0.5 ± 1.4	4.8 ± 17.0
12	Streptococcus genomospecies C8	1.88	2.3 ± 4.0	1.7 ± 2.8	1.5 ± 4.0
13	Streptococcus intermedius	1.81	1.9 ± 1.7	1.6 ± 2.3	1.9 ± 3.2
14	Gemella morbillorum	1.73	1.5 ± 1.7	2.4 ± 3.5	1.4 ± 1.7
15	Gemella haemolysans	1.63	1.9 ± 1.6	1.5 ± 1.7	1.4 ± 1.8
16	Streptococcus pneumoniae	1.63	1.8 ± 2.1	1.4 ± 2.2	1.6 ± 1.8
17	Filifactor alocis	1.48	0.2 ± 0.4	1.4 ± 2.9	3.4 ± 3.8
18	Granulicatella elegans	1.46	1.6 ± 1.6	1.6 ± 1.4	1.2 ± 1.4
19	Peptostreptococcus sp. oral clone BS044	1.46	1.3 ± 1.8	1.7 ± 1.9	1.4 ± 1.6
20	Veillonella atypica	1.42	1.6 ± 2.1	1.2 ± 2.2	1.4 ± 1.9
21	Streptococcus sp. oral clone 2056B	1.23	1.0 ± 1.4	1.6 ± 2.3	1.3 ± 2.0
22	Peptostreptococcus micros	1.19	1.9 ± 2.8	0.7 ± 1.7	0.7 ± 1.5
23	Neisseria elongata	1.17	1.4 ± 3.7	1.3 ± 1.9	0.6 ± 2.8
24	Streptococcus sp. oral strain 7A	1.08	0.9 ± 1.5	1.4 ± 1.7	1.4 ± 1.8
25	Selenomonas sputigena	0.98	0.8 ± 1.4	1.1 ± 2.2	1.1 ± 1.9
26	Streptococcus sp. oral clone FN051	0.96	0.7 ± 1.5	1.7 ± 2.2	0.7 ± 1.5
27	Capnocytophaga gingivalis	0.94	0.7 ± 0.9	0.9 ± 1.2	1.3 ± 1.5
28	Campylobacter concisus	0.90	1.3 ± 2.0	0.6 ± 1.0	0.6 ± 1.2
29	Selenomonas sp. oral clone EW051a	0.88	1.0 ± 1.4	0.1 ± 0.5	1.5 ± 2.2
30	Streptococcus anginosus	0.81	0.5 ± 0.9	0.6 ± 1.0	1.4 ± 1.3
31	Megasphaera sp. oral clone BB166	0.79	0.8 ± 1.2	0.9 ± 1.5	0.6 ± 1.0
32	Eikenella corrodens	0.73	0.8 ± 1.0	0.9 ± 1.0	0.6 ± 1.2
33	Dialister sp. oral clone E2_20	0.71	0.5 ± 1.0	1.1 ± 1.6	0.7 ± 1.1
34	Streptococcus genomospecies C7	0.67	0.6 ± 1.2	1.3 ± 2.3	0.2 ± 0.6
35	Neisseria sp. oral clone AP060	0.67	0.9 ± 1.7	0.9 ± 1.5	0.2 ± 0.8
36	Streptococcus salivarius	0.63	0.8 ± 1.8	0.3 ± 0.6	0.7 ± 1.4
37	Selenomonas sp. oral clone AA024	0.63	1.1 ± 2.5	0.3 ± 0.7	0.2 ± 0.8
38	Selenomonas sp. oral clone AJ036	0.63	0.6 ± 0.8	0.6 ± 1.0	0.6 ± 1.2
39	Streptococcus infantis	0.58	0.6 ± 1.0	0.5 ± 1.3	0.6 ± 1.0
40	Dialister sp. oral clone BS095	0.58	0.7 ± 1.0	0.4 ± 0.9	0.7 ± 0.8
41	Selenomonas noxia	0.56	0.7 ± 1.2	0.7 ± 0.9	0.3 ± 0.6
42	Gemella sanguinis	0.50	0.6 ± 1.9	0.6 ± 1.3	0.2 ± 0.4
43	Dialister pneumosintes	0.50	0.4 ± 0.8	0.4 ± 0.8	0.8 ± 1.1
44	Dialister invisus	0.50	0.7 ± 1.3	0.5 ± 0.9	0.2 ± 0.4
45	Selenomonas sp. oral clone DY027	0.48	0.5 ± 1.0	0.4 ± 0.9	0.5 ± 1.1
46	Selenomonas sp. oral clone DS051	0.48	0.4 ± 0.7	1.0 ± 1.7	0.1 ± 0.4
47	Selenomonas sp. oral clone IK004	0.46	0.3 ± 0.7	0.6 ± 1.7	0.5 ± 1.3
48	Veillonella sp. oral clone BU083	0.46	0.4 ± 0.9	0.2 ± 0.4	0.9 ± 1.9
49	Capnocytophaga granulosa	0.44	0.9 ± 1.4	0.1 ± 0.5	0.1 ± 0.3
50	Streptococcus sp. oral clone EK048	0.44	0.3 ± 0.8	0.6 ± 1.4	0.5 ± 0.8
51	Abiotrophia para-adiacens	0.42	0.6 ± 1.1	0.4 ± 0.8	0.2 ± 0.6
52	Abiotrophia sp. oral clone P4PA_155	0.42	0.5 ± 0.9	0.4 ± 0.8	0.5 ± 0.9
53	Streptococcus parasanguinis	0.42	0.4 ± 1.2	0.7 ± 1.9	0.2 ± 0.6
54	Selenomonas sp. oral clone DS071	0.42	0.1 ± 0.2	0.6 ± 1.2	0.8 ± 1.3
55	Selenomonas sp. oral clone EQ054	0.42	0.5 ± 1.2	0.4 ± 0.8	0.3 ± 0.6
56	Neisseria meningitidis	0.42	0.5 ± 0.8	0.2 ± 0.6	0.5 ± 0.8
57	Campylobacter rectus	0.42	0.1 ± 0.5	0.6 ± 1.0	0.7 ± 1.1
58	Rothia dentocariosa	0.40	0.6 ± 1.1	0.4 ± 0.9	0.1 ± 0.3
59	Streptococcus cristatus	0.40	0.3 ± 0.6	0.5 ± 0.9	0.4 ± 0.9
60	Selenomonas dianae	0.40	0.6 ± 0.9	0.1 ± 0.3	0.4 ± 0.8
61	Capnocytophaga sp. oral clone AH015	0.38	0.3 ± 0.4	0.6 ± 1.3	0.4 ± 0.8
62	Streptococcus sinensis	0.38	0.3 ± 0.6	0.3 ± 0.5	0.6 ± 0.8
63	Kingella oralis	0.38	0.3 ± 0.7	0.9 ± 1.2	0.0 ± 0.0
64	Neisseria denitrificans	0.38	0.4 ± 0.7	0.7 ± 1.3	0.1 ± 0.3
65	Enterococcus faecalis	0.35	0.6 ± 0.9	0.2 ± 0.6	0.1 ± 0.4
66	Eubacterium brachy	0.35	0.3 ± 0.7	0.6 ± 1.0	0.2 ± 0.6
67	Capnocytophaga sputigena	0.33	0.3 ± 0.7	0.5 ± 0.8	0.2 ± 0.6
68	Eubacterium sp. oral clone EW053	0.33	0.3 ± 1.0	0.4 ± 0.8	0.2 ± 0.6
69	Selenomonas sp. oral clone EW084	0.33	0.5 ± 0.1	0.2 ± 0.6	0.2 ± 0.6
70	Eubacterium saphenum	0.31	0.3 ± 0.8	0.1 ± 0.3	0.6 ± 1.0
71	Porphyromonas gingivalis	0.29	0.0 ± 0.0	0.2 ± 0.6	0.8 ± 2.4
72	Streptococcus agalactiae	0.29	0.3 ± 1.1	0.3 ± 0.8	0.2 ± 0.6
73	Selenomonas sp. oral clone DO042	0.29	0.2 ± 0.4	0.5 ± 0.9	0.3 ± 0.8
74	Streptococcus bovis	0.27	0.2 ± 0.4	0.5 ± 1.1	0.2 ± 0.4
75	Streptococcus suis	0.27	0.3 ± 0.5	0.1 ± 0.3	0.4 ± 0.8
76	Peptostreptococcus sp. oral clone CK035	0.27	0.4 ± 0.9	0.1 ± 0.3	0.3 ± 0.8
77	Selenomonas-like sp. oral clone CS015	0.27	0.1 ± 0.2	0.3 ± 0.7	0.5 ± 0.8
78	Selenomonas sp. oral clone CS002	0.27	0.1 ± 0.2	0.6 ± 1.3	0.2 ± 0.6
79	Corynebacterium matruchotii	0.25	0.2 ± 0.4	0.4 ± 0.9	0.1 ± 0.5
80	Streptococcus sp. oral clone 4093B	0.25	0.2 ± 0.7	0.3 ± 0.8	0.3 ± 0.5
81	Streptococcus sp. oral clone FX003	0.25	0.3 ± 0.6	0.1 ± 0.5	0.4 ± 0.9
82	Eubacterium sp. oral clone E1-K17	0.25	0.3 ± 0.7	0.2 ± 0.4	0.2 ± 0.6
83	Treponema sp. strain Smibert-5	0.25	0.2 ± 0.4	0.2 ± 0.8	0.4 ± 0.9
84	Atopobium rimae	0.23	0.4 ± 0.9	0.0 ± 0.0	0.2 ± 0.6
85	Streptococcus pyogenes	0.23	0.3 ± 0.8	0.3 ± 0.6	0.1 ± 0.4
86	Desulfobulbus sp. oral clone CH031	0.23	0.3 ± 0.8	0.0 ± 0.0	0.4 ± 1.2
87	Peptostreptococcus sp. oral clone MDA2346-2	0.23	0.0 ± 0.0	0.3 ± 0.6	0.5 ± 1.2
88	Selenomonas sp. oral clone CS024	0.23	0.4 ± 0.8	0.3 ± 0.0	0.3 ± 0.6
89	Selenomonas sp. oral clone GT010	0.23	0.5 ± 1.4	0.1 ± 0.0	0.1 ± 0.5
90	Selenomonas lacticifex	0.23	0.6 ± 1.6	0.0 ± 0.0	0.0 ± 0.0
91	Alysiella filiformis	0.23	0.0 ± 0.0	0.8 ± 1.9	0.0 ± 0.0
92	Lautropia sp. oral clone AP009	0.23	0.1 ± 0.2	0.7 ± 1.3	0.0 ± 0.0
93	Granulicatella adiacens	0.21	0.3 ± 0.6	0.2 ± 0.6	0.1 ± 0.5
94	Gemella sp. strain 1754-94	0.21	0.1 ± 0.3	0.0 ± 0.0	0.6 ± 0.9
95	Streptococcus intestinalis	0.21	0.3 ± 0.8	0.2 ± 0.6	0.1 ± 0.3
96	Streptococcus mutans	0.21	0.2 ± 0.7	0.1 ± 0.4	0.3 ± 0.6
97	Streptococcus peroris	0.21	0.2 ± 0.4	0.1 ± 0.5	0.4 ± 0.7
98	Catonella sp. oral clone FL037	0.21	0.3 ± 0.8	0.0 ± 0.0	0.4 ± 0.9
99	Catonella morbi	0.21	0.1 ± 0.3	0.4 ± 0.6	0.2 ± 0.6
100	Selenomonas noxia-like sp. oral clone CI002	0.21	0.5 ± 1.1	0.0 ± 0.0	0.1 ± 0.3
101	Selenomonas sp. oral clone GI064	0.21	0.0 ± 0.0	0.7 ± 0.2	0.0 ± 0.0
102	Neisseria flava	0.21	0.3 ± 0.8	0.1 ± 0.4	0.2 ± 0.8
103	Campylobacter hominis	0.21	0.2 ± 0.5	0.4 ± 0.9	0.0 ± 0.0
104	Corynebacterium sp. oral clone AK153	0.19	0.2 ± 0.5	0.4 ± 0.9	0.0 ± 0.0
105	Streptococcus hyointestinalis	0.19	0.0 ± 0.0	0.2 ± 0.6	0.4 ± 0.9
106	Streptococcus sp. oral clone CH016	0.19	0.1 ± 0.2	0.5 ± 0.8	0.1 ± 0.3
107	Streptococcus sp. oral clone BM035	0.19	0.4 ± 0.8	0.0 ± 0.0	0.1 ± 0.5
108	Eubacterium saburreum	0.19	0.4 ± 0.8	0.1 ± 0.3	0.0 ± 0.0
109	Megasphaera micronuciformis	0.19	0.1 ± 0.5	0.2 ± 0.6	0.3 ± 0.8
110	Selenomonas sp. oral clone EW076	0.19	0.3 ± 0.6	0.1 ± 0.3	0.2 ± 0.4
111	Selenomonas sp. oral clone DD020	0.19	0.3 ± 0.6	0.1 ± 0.5	0.1 ± 0.5
112	Veillonella parvula	0.19	0.1 ± 0.3	0.2 ± 0.6	0.3 ± 0.6
113	Neisseria genomospecies P1 clone P4PC_20	0.19	0.4 ± 1.1	0.0 ± 0.0	0.1 ± 0.4
114	Neisseria pharyngis	0.19	0.3 ± 0.6	0.0 ± 0.0	0.2 ± 0.4
115	Deferribacteres sp. oral clone BH007	0.17	0.0 ± 0.0	0.4 ± 0.9	0.1 ± 0.4
116	Streptococcus didelphis	0.17	0.4 ± 0.9	0.1 ± 0.3	0.1 ± 0.3
117	Streptococcus oligofermentans	0.17	0.1 ± 0.2	0.4 ± 0.6	0.1 ± 0.4
118	Streptococcus sp. oral clone 3097C	0.17	0.1 ± 0.2	0.1 ± 0.5	0.4 ± 0.6
119	Streptococcus sp. oral clone AY020	0.17	0.3 ± 0.6	0.1 ± 0.4	0.1 ± 0.3
120	Streptococcus sp. oral clone BW009	0.17	0.4 ± 0.8	0.0 ± 0.0	0.0 ± 0.0
121	Catonella sp. oral clone EZ006	0.17	0.1 ± 0.2	0.2 ± 0.8	0.3 ± 0.8
122	Johnsonella ignava	0.17	0.2 ± 0.7	0.3 ± 0.8	0.0 ± 0.0
123	Selenomonas sp. oral clone EW079	0.17	0.2 ± 0.5	0.1 ± 0.4	0.2 ± 0.6
124	Veillonella dispar	0.17	0.2 ± 0.4	0.1 ± 0.5	0.2 ± 0.4
125	Treponema sp. strain VI:G:G47	0.17	0.0 ± 0.0	0.1 ± 0.5	0.4 ± 0.9
126	Treponema sp. strain V:19:D36	0.17	0.0 ± 0.0	0.3 ± 0.7	0.3 ± 0.8
127	Deferribacteres sp. oral clone BA121	0.15	0.2 ± 0.7	0.2 ± 1.0	0.0 ± 0.0
128	Gemella sp. oral strain C24KA	0.15	0.1 ± 0.3	0.2 ± 0.6	0.1 ± 0.4
129	Streptococcus sp. oral clone 2061A	0.15	0.1 ± 0.2	0.1 ± 0.3	0.4 ± 0.9
130	Streptococcus uberis	0.15	0.1 ± 0.2	0.3 ± 0.6	0.1 ± 0.4
131	Dialister sp. oral strain GBA27	0.15	0.2 ± 0.4	0.2 ± 0.4	0.1 ± 0.3
132	Eubacterium sp. oral clone EI074	0.15	0.1 ± 0.3	0.3 ± 0.6	0.1 ± 0.5
133	Eubacterium sp. oral clone DO008	0.15	0.1 ± 0.3	0.0 ± 0.0	0.4 ± 1.2
134	Eubacterium sp. oral clone IR009	0.15	0.2 ± 0.7	0.1 ± 0.3	0.1 ± 0.5
135	Megasphaera sp. oral clone BU057	0.15	0.2 ± 0.5	0.1 ± 0.5	0.1 ± 0.4
136	Selenomonas-like sp. oral strain FNA3	0.15	0.3 ± 0.7	0.0 ± 0.0	0.1 ± 0.3

↵ a The 136 most common species are listed here. For a complete listing of all 260 species detected, see Table S1A in the supplemental material.
↵ b Values are means of baseline and 24-month samples.

Additional Files

Figures
Tables

Supplemental material

Files in this Data Supplement:

Supplemental file 1 - Table S1A, showing data for all 260 species and phylotypes detected (a partial list of species appears in Table 1 of this study).
MS Word document, 397K.