Diversity and dynamics of rare and of resident bacterial populations in coastal sands - PubMed (original) (raw)

Diversity and dynamics of rare and of resident bacterial populations in coastal sands

Angélique Gobet et al. ISME J. 2012 Mar.

Abstract

Coastal sands filter and accumulate organic and inorganic materials from the terrestrial and marine environment, and thus provide a high diversity of microbial niches. Sands of temperate climate zones represent a temporally and spatially highly dynamic marine environment characterized by strong physical mixing and seasonal variation. Yet little is known about the temporal fluctuations of resident and rare members of bacterial communities in this environment. By combining community fingerprinting via pyrosequencing of ribosomal genes with the characterization of multiple environmental parameters, we disentangled the effects of seasonality, environmental heterogeneity, sediment depth and biogeochemical gradients on the fluctuations of bacterial communities of marine sands. Surprisingly, only 3-5% of all bacterial types of a given depth zone were present at all times, but 50-80% of them belonged to the most abundant types in the data set. About 60-70% of the bacterial types consisted of tag sequences occurring only once over a period of 1 year. Most members of the rare biosphere did not become abundant at any time or at any sediment depth, but varied significantly with environmental parameters associated with nutritional stress. Despite the large proportion and turnover of rare organisms, the overall community patterns were driven by deterministic relationships associated with seasonal fluctuations in key biogeochemical parameters related to primary productivity. The maintenance of major biogeochemical functions throughout the observation period suggests that the small proportion of resident bacterial types in sands perform the key biogeochemical processes, with minimal effects from the rare fraction of the communities.

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Figures

Figure 1

Figure 1

Microbial community distribution in the sand and the water column. (a) From top to bottom: acridine orange staining of bacteria in the water column, the pore water and on the surface of a sand grain (scale bar=50 μm). (b) Relative number of sequences in different compartments for the top 5-cm sand layer and in the overlying water column in April 2008. Here, the phylum level was chosen for illustrative purposes. (c) Sequence distribution in the sand over time, in which each bar represents an OTUunique (only OTUunique occurring more than 100 times in the whole data set are shown). The Proteobacteria phylum was further split into its corresponding classes, for example, Alpha, Gamma, Delta; Cy, Cyanobacteria; Ba, Bacteroidetes; Aci, Acidobacteria; Others: Actinobacteria, NA, not annotated Proteobacteria, Planctomycetes, Chloroflexi, Verrucomicrobia, WS3, Firmicutes, Lentisphaerae, Deferribacteres and Gemmatimonadetes.

Figure 2

Figure 2

Bacterial community turnover between two consecutive depth layers (a) or sampling times (b). The percentage of OTU shared between a sampling depth (or date) and the previous one was calculated after PyroNoise correction and OTU clustering of the 454 MPTS data set at several levels of sequence dissimilarity. Bars correspond to s.d. calculated over 4–6 sampling dates (a) or three depth layers (b), except for July and November 2005 in which two depth layers were considered. The first depth layer and sampling date (February 2005) are indicated by the grey point as 100% of OTU. OTUall represents the original data set with all OTUunique. It is used here as a reference data set to study the effects of various correction levels on the observed dynamics of the bacterial community composition.

Figure 3

Figure 3

Distribution of the maximum abundance of (a) SSOrel (i.e., those OTU0% that, at least in one sample, consisted of only one sequence) and (b) resident OTU0% (i.e., OTU0% present at all times) in the top 10-cm layer. In (a), panels 1, 2 and 3 are examples of cases, in which particular high fluctuations from the single-sequence case (white arrow) to higher-sequence abundances were observed. In (b), panels 1, 2, 3 illustrate cases of particularly high fluctuations in relative abundances (no absolute abundances were calculated in this case). All data were initially processed to remove pyrosequencing noise. Rel. abundance, relative abundance to the total number of sequences per sampling time: February 2005 (13 285), April 2005 (7902), July 2005 (10 910), November 2005 (21 931), 1 March 2006 (17 302), 2 March 2006 (17 897).

Figure 4

Figure 4

Environmental factors associated with variations of the bacterial community structure at the phylum level. Pearson's ρ indicates correlations between phylum sequence abundance and several environmental parameters. For example, a red square between sediment depth and Chloroflexi indicates a higher number of sequences with increasing depth; nonsignificant relationships between water temperature and sequence variation in any of the bacterial groups are indicated by white squares; a blue square between chlorophyll a and Chloroflexi denotes a decrease in sequences as chlorophyll a concentration gets higher (the latter being concordant with the relationship between increasing depth and Chloroflexi sequences number). The Proteobacteria phylum level was separated into its corresponding classes to obtain a higher resolution. NA-Proteobacteria are the Proteobacteria with missing class annotation. The total number of sequences in each phylum is indicated in parentheses. SiO2, silicate; PO4, phosphate; NO2, nitrite; NO3, nitrate; NH4, ammonium; Chl a, chlorophyll a; Pheo, pheophytin; BCC, bacterial abundance; Bprod, bacterial carbon production; Chit, chitinase; α-glu, α-glucosidase; β-glu, β-glucosidase; Lip, lipase; Amin, aminopeptidase; Phos, phosphatase.

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