Johanna Sjöstedt

Recruitment of Members from the Rare Biosphere of Marine Bacterioplankton Communities after an Environmental Disturbance

ABSTRACT A bacterial community may be resistant to environmental disturbances if some of its species show metabolic flexibility and physiological tolerance to the changing conditions. Alternatively, disturbances can change the composition of the community and thereby potentially affect ecosystem processes. The impact of disturbance on the composition of bacterioplankton communities was examined in continuous seawater cultures. Bacterial assemblages from geographically closely connected areas, the Baltic Sea (salinity 7 and high dissolved organic carbon [DOC]) and Skagerrak (salinity 28 and low DOC), were exposed to gradual opposing changes in salinity and DOC over a 3-week period such that the Baltic community was exposed to Skagerrak salinity and DOC and vice versa. Denaturing gradient gel electrophoresis and clone libraries of PCR-amplified 16S rRNA genes showed that the composition of the transplanted communities differed significantly from those held at constant salinity. Despite this, the growth yields (number of cells ml−1) were similar, which suggests similar levels of substrate utilization. Deep 454 pyrosequencing of 16S rRNA genes showed that the composition of the disturbed communities had changed due to the recruitment of phylotypes present in the rare biosphere of the original community. The study shows that members of the rare biosphere can become abundant in a bacterioplankton community after disturbance and that those bacteria can have important roles in maintaining ecosystem processes.

Local Environmental Conditions Shape Generalist But Not Specialist Components of Microbial Metacommunities in the Baltic Sea

Marine microbes exhibit biogeographical patterns linked with fluxes of matter and energy. Yet, knowledge of the mechanisms shaping bacterioplankton community assembly across temporal scales remains poor. We examined bacterioplankton 16S rRNA gene fragments obtained from Baltic Sea transects to determine phylogenetic relatedness and assembly processes coupled with niche breadth. Communities were phylogenetically more related over time than expected by chance, albeit with considerable temporal variation. Hence, habitat filtering, i.e., local environmental conditions, rather than competition structured bacterioplankton communities in summer but not in spring or autumn. Species sorting (SS) was the dominant assembly process, but temporal and taxonomical variation in mechanisms was observed. For May communities, Cyanobacteria, Actinobacteria, Alpha- and Betaproteobacteria exhibited SS while Bacteroidetes and Verrucomicrobia were assembled by SS and mass effect. Concomitantly, Gammaproteobacteria were assembled by the neutral model and patch dynamics. Temporal variation in habitat filtering and dispersal highlights the impact of seasonally driven reorganization of microbial communities. Typically abundant Baltic Sea populations such as the NS3a marine group (Bacteroidetes) and the SAR86 and SAR11 clade had the highest niche breadth. The verrucomicrobial Spartobacteria population also exhibited high niche breadth. Surprisingly, variation in bacterioplankton community composition was regulated by environmental factors for generalist taxa but not specialists. Our results suggest that generalists such as NS3a, SAR86, and SAR11 are reorganized to a greater extent by changes in the environment compared to specialists and contribute more strongly to determining overall biogeographical patterns of marine bacterial communities.

Disentangling seasonal bacterioplankton population dynamics by high‐frequency sampling

Multiyear comparisons of bacterioplankton succession reveal that environmental conditions drive community shifts with repeatable patterns between years. However, corresponding insight into bacterioplankton dynamics at a temporal resolution relevant for detailed examination of variation and characteristics of specific populations within years is essentially lacking. During 1 year, we collected 46 samples in the Baltic Sea for assessing bacterial community composition by 16S rRNA gene pyrosequencing (nearly twice weekly during productive season). Beta-diversity analysis showed distinct clustering of samples, attributable to seemingly synchronous temporal transitions among populations (populations defined by 97% 16S rRNA gene sequence identity). A wide spectrum of bacterioplankton dynamics was evident, where divergent temporal patterns resulted both from pronounced differences in relative abundance and presence/absence of populations. Rates of change in relative abundance calculated for individual populations ranged from 0.23 to 1.79 day(-1) . Populations that were persistently dominant, transiently abundant or generally rare were found in several major bacterial groups, implying evolution has favoured a similar variety of life strategies within these groups. These findings suggest that high temporal resolution sampling allows constraining the timescales and frequencies at which distinct populations transition between being abundant or rare, thus potentially providing clues about physical, chemical or biological forcing on bacterioplankton community structure.

Transplant experiments uncover Baltic Sea basin-specific responses in bacterioplankton community composition and metabolic activities

Anthropogenically induced changes in precipitation are projected to generate increased river runoff to semi-enclosed seas, increasing loads of terrestrial dissolved organic matter and decreasing salinity. To determine how bacterial community structure and functioning adjust to such changes, we designed microcosm transplant experiments with Baltic Proper (salinity 7.2) and Bothnian Sea (salinity 3.6) water. Baltic Proper bacteria generally reached higher abundances than Bothnian Sea bacteria in both Baltic Proper and Bothnian Sea water, indicating higher adaptability. Moreover, Baltic Proper bacteria growing in Bothnian Sea water consistently showed highest bacterial production and beta-glucosidase activity. These metabolic responses were accompanied by basin-specific changes in bacterial community structure. For example, Baltic Proper Pseudomonas and Limnobacter populations increased markedly in relative abundance in Bothnian Sea water, indicating a replacement effect. In contrast, Roseobacter and Rheinheimera populations were stable or increased in abundance when challenged by either of the waters, indicating an adjustment effect. Transplants to Bothnian Sea water triggered the initial emergence of particular Burkholderiaceae populations, and transplants to Baltic Proper water triggered Alteromonadaceae populations. Notably, in the subsequent re-transplant experiment, a priming effect resulted in further increases to dominance of these populations. Correlated changes in community composition and metabolic activity were observed only in the transplant experiment and only at relatively high phylogenetic resolution. This suggested an importance of successional progression for interpreting relationships between bacterial community composition and functioning. We infer that priming effects on bacterial community structure by natural episodic events or climate change induced forcing could translate into long-term changes in bacterial ecosystem process rates.

Abundance of Broad Bacterial Taxa in the Sargasso Sea Explained by Environmental Conditions but Not Water Mass

ABSTRACT To explore the potential linkage between distribution of marine bacterioplankton groups, environmental conditions, and water mass, we investigated the factors determining the abundance of bacterial taxa across the hydrographically complex Subtropical Convergence Zone in the Sargasso Sea. Based on information from 16S rRNA gene clone libraries from various locations and two depths, abundances of the predominant taxa (eubacteria, Archaea, Alphaproteobacteria, Gammaproteobacteria, Bacteroidetes, and the Roseobacter, SAR11, and SAR86 clades) were quantified by real-time PCR. In addition, the abundances of Synechococcus, Prochlorococcus, and picoalgae were determined by flow cytometry. Linear multiple-regression models determining the relative effects of eight environmental variables and of water mass explained 35 to 86% of the variation in abundance of the quantified taxa, even though only one to three variables were significantly related to any particular taxons abundance. Most of the variation in abundance was explained by depth and chlorophyll a. The predominant phototrophs, Prochlorococcus and picoalgae, were negatively correlated with phosphate, whereas eubacteria, heterotrophic bacteria, and SAR86 were negatively correlated with nitrite. Water mass showed limited importance for explaining the abundance of the taxonomical groups (significant only for Roseobacter, explaining 14% of the variation). The results suggest the potential for predicting the abundance of broad bacterioplankton groups throughout the Sargasso Sea using only a few environmental parameters.

Metapopulation theory identifies biogeographical patterns among core and satellite marine bacteria scaling from tens to thousands of kilometers.

Metapopulation theory developed in terrestrial ecology provides applicable frameworks for interpreting the role of local and regional processes in shaping species distribution patterns. Yet, empirical testing of metapopulation models on microbial communities is essentially lacking. We determined regional bacterioplankton dynamics from monthly transect sampling in the Baltic Sea Proper using 16S rRNA gene sequencing. A strong positive trend was found between local relative abundance and occupancy of populations. Notably, the occupancy-frequency distributions were significantly bimodal with a satellite mode of rare endemic populations and a core mode of abundant cosmopolitan populations (e.g. Synechococcus, SAR11 and SAR86 clade members). Temporal changes in population distributions supported several theoretical frameworks. Still, bimodality was found among bacterioplankton communities across the entire Baltic Sea, and was also frequent in globally distributed datasets. Datasets spanning waters with widely different physicochemical characteristics or environmental gradients typically lacked significant bimodal patterns. When such datasets were divided into subsets with coherent environmental conditions, bimodal patterns emerged, highlighting the importance of positive feedbacks between local abundance and occupancy within specific biomes. Thus, metapopulation theory applied to microbial biogeography can provide novel insights into the mechanisms governing shifts in biodiversity resulting from natural or anthropogenically induced changes in the environment.

Bimodal occupancy-frequency distributions uncover the importance of regional dynamics in shaping marine microbial biogeography

Metapopulation theory developed in terrestrial ecology provides applicable frameworks for interpreting the role of local and regional processes in shaping species distribution patterns. Yet, empirical testing of metapopulation models on microbial communities is essentially lacking. Here we determined regional bacterioplankton dynamics from monthly transect sampling in the Baltic Sea Proper (16 sites, 11 occasions, 2010-2011) using 16S rRNA gene pyrosequencing. A strong positive correlation was found between local relative abundance and occupancy of populations. Notably, the occupancy-frequency distributions (the number of populations occupying different number of sites) were significantly bimodal with a satellite mode of mostly rare endemic populations and a core mode of abundant cosmopolitan populations (e.g. Synechococcus, SAR11 and SAR86 clade members). Observed temporal changes in population distributions supported theoretical predictions that stochastic variation in local extinction and colonization rates accounted for observed bimodality. Moreover, bimodality was found for bacterioplankton across the entire Baltic Sea, and was also frequent in globally distributed datasets where average Bray-Curtis distances were significantly different between bimodal and non-bimodal datasets. Still, datasets spanning waters with distinct physicochemical characteristics or environmental gradients, e.g. brackish and marine or surface to deep waters, typically lacked significant bimodal patterns. When such datasets were divided into subsets with coherent environmental conditions, bimodal patterns emerged, highlighting the importance of positive feedbacks between local abundance and occupancy within specific biomes. Thus, metapopulation theory applied to microbial biogeography can provide novel insights into the mechanisms governing shifts in biodiversity resulting from natural or anthropogenically induced changes in the environment. Significance statement Marine bacteria regulate global cycles of elements essential to life and respond rapidly to environmental change. Yet, the ecological factors that determine distribution and activity patterns of microbial populations across different spatial scales and environmental gradients remain basically unconstrained. Our metapopulation model-based analyses show that dispersal-driven processes contribute to structuring the biogeography of marine microorganisms from small to large geographical areas. Discovery of bimodal distribution patterns pinpointed satellite microbial populations with highly restricted ranges and defined abundant core populations widely distributed in coherence with environmental conditions. Thus, application of metapopulation models on microbial community structure may allow the definition of biogeographic regions critical for interpreting the outcome of future ocean changes. Classification Biological Sciences, Environmental Sciences