Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters

Abstract

Marine Archaea are important players among microbial plankton and significantly contribute to biogeochemical cycles, but details regarding their community structure and long-term seasonal activity and dynamics remain largely unexplored. In this study, we monitored the interannual archaeal community composition of abundant and rare biospheres in northwestern Mediterranean Sea surface waters by pyrosequencing 16S rDNA and rRNA. A detailed analysis of the rare biosphere structure showed that the rare archaeal community was composed of three distinct fractions. One contained the rare Archaea that became abundant at different times within the same ecosystem; these cells were typically not dormant, and we hypothesize that they represent a local seed bank that is specific and essential for ecosystem functioning through cycling seasonal environmental conditions. The second fraction contained cells that were uncommon in public databases and not active, consisting of aliens to the studied ecosystem and representing a nonlocal seed bank of potential colonizers. The third fraction contained Archaea that were always rare but actively growing; their affiliation and seasonal dynamics were similar to the abundant microbes and could not be considered a seed bank. We also showed that the major archaeal groups, Thaumarchaeota marine group I and Euryarchaeota group II.B in winter and Euryarchaeota group II.A in summer, contained different ecotypes with varying activities. Our findings suggest that archaeal diversity could be associated with distinct metabolisms or life strategies, and that the rare archaeal biosphere is composed of a complex assortment of organisms with distinct histories that affect their potential for growth.

Fig. 1.

16S rDNA against 16S rRNA OTUs frequencies for abundant OTUs when they are abundant (A) and when they become rare (B). The RNA and DNA frequencies are plotted against each other for all abundant OTUs and all time points. The black line represents the regression, and the dotted line is the 1:1 line.

Fig. 2.

Distribution of the percent identity from a comparison between public database sequences (SILVA) and abundant 16S rDNA and rRNA sequences (A) and always-rare 16S rDNA and rRNA sequences (B). The data are fitted to a model of normal distributions (black lines) that identifies groups of OTUs as common (i.e., a high percentage identity) or uncommon (i.e., a low percentage identity).

Fig. 3.

Seasonal dynamics of the most abundant taxonomic groups in both the 16S rDNA and rRNA sequence datasets: (A) MGI, (B) MGII.A, and (C) MGII.B. Winter months are shown in gray; summer months are shown in white.

Fig. 4.

Seasonal dynamics of active (16S rRNA dataset) MGI clusters: MGI.A, MGI.B, MGI.C, and MGI.D. Winter months are shown in gray; summer months are shown in white.