Individual Physiological Adaptations Enable Selected Bacterial Taxa To Prevail during Long-Term Incubations

Abstract

Enclosure experiments are frequently used to investigate the impact of changing environmental conditions on microbial assemblages. Yet, how the incubation itself challenges complex bacterial communities is thus far unknown. In this study, metaproteomic profiling, 16S rRNA gene analyses, and cell counts were combined to evaluate bacterial communities derived from marine, mesohaline, and oligohaline conditions after long-term batch incubations. Early in the experiment, the three bacterial communities were highly diverse and differed significantly in their compositions. Manipulation of the enclosures with terrigenous dissolved organic carbon resulted in notable differences compared to the control enclosures at this early phase of the experiment. However, after 55 days, bacterial communities in the manipulated and the control enclosures under marine and mesohaline conditions were all dominated by gammaproteobacterium Spongiibacter. In the oligohaline enclosures, actinobacterial cluster I of the hgc group (hgc-I) remained abundant in the late phase of the incubation. Metaproteome analyses suggested that the ability to use outer membrane-based internal energy stores, in addition to the previously described grazing resistance, may enable the gammaproteobacterium Spongiibacter to prevail in long-time incubations. Under oligohaline conditions, the utilization of external recalcitrant carbon appeared to be more important (hgc-I). Enclosure experiments with complex natural microbial communities are important tools to investigate the effects of manipulations. However, species-specific properties, such as individual carbon storage strategies, can cause manipulation-independent effects and need to be considered when interpreting results from enclosures. IMPORTANCE In microbial ecology, enclosure studies are often used to investigate the effect of single environmental factors on complex bacterial communities. However, in addition to the manipulation, unintended effects ("bottle effect") may occur due to the enclosure itself. In this study, we analyzed the bacterial communities that originated from three different salinities of the Baltic Sea, comparing their compositions and physiological activities both at the early stage and after 55 days of incubation. Our results suggested that internal carbon storage strategies impact the success of certain bacterial species, independent of the experimental manipulation. Thus, while enclosure experiments remain valid tools in environmental research, microbial community composition shifts must be critically followed. This investigation of the metaproteome during long-term batch enclosures expanded our current understanding of the so-called "bottle effect," which is well known to occur during enclosure experiments.

Metagenomics assessment of Anthropogenic impact on coral reef-associated microorganisms on the Kenyan Indian Ocean

“…These similarities suggests that the influence of coral reefs' primary productivity on taxonomic richness and diversity (Claire et al, 2003;Silveira et al, 2017) As for differential COG enrichment, predicted proteins for amino acid transport and metabolism were significantly overrepresented in the Tara Oceans metagenomes. This is in agreement with the most abundant marine microbial communities, especially members of class Alphaproteobacteria, that express disproportionate abundance of high-affinity transporters under oligotrophic conditions (Herlemann et al, 2019). Signal transduction histidine kinase which enables microbes to sense, respond, and adapt to a wide range of environments, stressors, and growth conditions (Skerker et al, 2005) were significantly enriched in the reef metagenomes.…”

Resistance of freshwater sediment bacterial communities to salinity disturbance and the implication for industrial salt discharge and climate change-based salinization

“…The abundance of Hydrogenophaga, a genus containing many hydrogen-oxidizing bacteria, increased with increased salinity. In contrast, the abundance of the HGC-I OTU was high in natural sites, except the pond, but was significantly lower in the experiment, as this bacterial group is known to be sensitive to artificial environments (Herlemann et al, 2019).…”

“…However, a decrease in the water bacterial richness was observed in parallel in all aquaria, including in the reference. This was a reaction to the confined artificial aquaria conditions where there was an altered nutrient availability (Ionescu et al, 2015;Herlemann et al, 2017;Herlemann et al, 2019) and different grazing patterns of bacteria by ciliates and heterotrophic nanoflagellates (Ionescu et al, 2015;Herlemann et al, 2019). A significantly stronger dynamic of bacterial richness was observed for the more intense manipulation (i.e., SAL6 and AB) supporting a sensitivity of the water bacterial richness to pulse disturbance in addition to confinement stress.…”

Distinct stages of the intestinal bacterial community of Ampullaceana balthica after salinization

“…A decline in bacterial richness and changes in the bacterial community composition due to an organism’s transfer from natural conditions to aquaria settings has been observed previously ( Pratte et al, 2015 ; Kivistik et al, 2020 ). The changes in bacterial communities due to the transfer to closed systems have been ascribed to grazing ( Jürgens and Güde, 1994 ), changes in the carbon quality ( Herlemann et al, 2014 ), missing replacement of bacteria ( Ionescu et al, 2015 ), alternative strategies to acquire carbon ( Herlemann et al, 2019 ), and accumulation of toxic metabolites. In addition, the change in the conditions of the host due to the shift from a river environment to a pond-like environment in the aquarium could influence the bacterial richness.…”