Annual dynamics of North Sea bacterioplankton: seasonal variability superimposes short-term variation

Abstract

The dynamics of coastal marine microbial communities are driven by seasonally changing abiotic and biotic factors as well as by rapidly occurring short-term changes such as river fresh water influxes or phytoplankton blooms. We examined the variability of the free-living bacterioplankton at Helgoland Roads (German Bight, North Sea) over a period of one year with high temporal and taxonomic resolution to reveal variation patterns and main influencing factors. 16S rRNA gene tag sequencing of the bacterioplankton community hints at annual recurrence and resilience of few main taxa belonging to Alphaproteobacteria, Betaproteobacteria, Flavobacteriia, Acidimicrobiia and Thermoplasmata. Multiple regression analyses with various environmental factors revealed changes in water current patterns and resulting phytoplankton blooms as the main driving factors for short-term variation and temperature as the overlying factor for seasonal variation. Comparison of bacterioplankton successions during spring and summer phytoplankton blooms revealed the same dominating Flavobacteriia operational taxonomic units (OTUs) but shifts in Roseobacter related OTUs (Alphaproteobacteria) and SAR92 clade members (Gammaproteobacteria). Network analysis suggests that during spring and summer phytoplankton blooms temperature-dependent guilds are formed. In conclusion, our data imply that short-term bacterioplankton successions in response to phytoplankton blooms are indirectly affected by temperature, which is a major niche-defining factor in the German Bight.

Spatiotemporal variation of the bacterioplankton community in the German Bight: from estuarine to offshore regions

“…and thus, has potentially strong influence on the diversity. This is also supported by a recent study on the annual bacterial dynamics at Helgoland Roads [27]. The authors suggest that temperature constitutes a major factor for the formation of ecological niches in the German Bight and indirectly affects short-term bacterial succession in response to phytoplankton blooms.…”

“…Here we present a comprehensive spatiotemporal annual survey of the bacterioplankton community along a 100 km transect in the German Bight (North Sea) reaching from brackish waters (Elbe estuary) to offshore sites and link it with environmental parameters. This extensive analysis of the mechanisms that drive the spatiotemporal variation patterns in the German Bight adds to the knowledge that has been gained during a comprehensive annual survey on the bacterial community composition at Helgoland Roads using 16S rRNA gene tag sequencing [27]. In combination both studies draw a comprehensive, detailed picture of the variation patterns of the bacterial community in the German Bight.…”

“…Therefore, we propose that a strong influence of phytoplankton on the bacterioplankton community composition is restricted to short time scales during phytoplankton blooms and is of minor importance for the overall long-term patterns in community composition such as resilience and recurrence. This assumption is supported by an 16S rRNA gene tag sequencing based annual survey on the bacterioplankton community at Helgoland Roads that reported a rapidly changing community composition during phytoplankton blooms which was overwhelmed by temperature-driven seasonal variation [27]. However, interdependencies between phyto-and bacterioplankton cannot easily be disentangled since growth of both organism groups rely to some extent on the same environmental triggers (temperature, nutrients) and also interact (via exudates) or compete (nutrients) [4].…”

“…Seasonal shifts in bacterial community composition (BCC) are substantially driven by changes in temperature and nutrient concentrations [2,13]. Multi-annual studies revealed that recurrence of bacterial community structure is predictable from ocean environmental conditions such as temperature and day length for instance [10,14,27]. However, marine habitats represent continuous, highly connected environments, where changes in bacterial communities are complex and triggered by temporal and spatial components simultaneously.…”

“…Seasonal variation was demonstrated on different time scales covering several months to multiple years using fingerprint methods like ribosomal intergenic spacer analysis (RISA), denaturing gradient gel electrophoresis (DGGE) and 16S rRNA gene tag sequencing [12,27,36]. The authors linked variation in community composition with various environmental parameters and revealed temperature and phytoplankton abundance as main driving forces.…”