Comparative proteomics reveals signature metabolisms of exponentially growing and stationary phase marine bacteria

Muthusamy, Sarala Devi; Lundin, Daniel; Branca, Rui M.; Baltar, Federico; González, José M.; Lehtiö, Janne; Pinhassi, Jarone

doi:10.1111/1462-2920.13725

Cited by 31 publications

(26 citation statements)

References 68 publications

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“…This suggests that T. roseum uses CO to supplement available organic carbon during growth (mixotrophy) and persistence. These findings are broadly similar to observations made in other phyla, notably Actinobacteria and Proteobacteria, that hydrogenase and carbon monoxide dehydrogenase expression are induced by organic carbon limitation [28, 31, 60–64].…”

Section: Resultssupporting

confidence: 89%

“…Indeed, various heterotrophic bacteria have previously been inferred to be capable of oxidising atmospheric CO, including Proteobacteria [80–83], Actinobacteria [84, 85], and a Thermogemmatispora strain [12]. Moreover, other datasets have shown that carbon monoxide dehydrogenase expression is activated during nutrient limitation in other aerobic organisms [60–64]. However, in contrast to atmospheric H 2 [29, 32], it remains to be validated through genetic and biochemical studies that atmospheric CO oxidation can enhance survival of bacteria during persistence.…”

Section: Resultsmentioning

confidence: 99%

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Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

et al. 2019

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Most aerobic bacteria exist in dormant states within natural environments. In these states, they endure adverse environmental conditions such as nutrient starvation by decreasing metabolic expenditure and using alternative energy sources. In this study, we investigated the energy sources that support persistence of two aerobic thermophilic strains of the environmentally widespread but understudied phylum Chloroflexi. A transcriptome study revealed that Thermomicrobium roseum (class Chloroflexia) extensively remodels its respiratory chain upon entry into stationary phase due to nutrient limitation. Whereas primary dehydrogenases associated with heterotrophic respiration were downregulated, putative operons encoding enzymes involved in molecular hydrogen (H2), carbon monoxide (CO), and sulfur compound oxidation were significantly upregulated. Gas chromatography and microsensor experiments showed that T. roseum aerobically respires H2 and CO at a range of environmentally relevant concentrations to sub-atmospheric levels. Phylogenetic analysis suggests that the hydrogenases and carbon monoxide dehydrogenases mediating these processes are widely distributed in Chloroflexi genomes and have probably been horizontally acquired on more than one occasion. Consistently, we confirmed that the sporulating isolate Thermogemmatispora sp. T81 (class Ktedonobacteria) also oxidises atmospheric H2 and CO during persistence, though further studies are required to determine if these findings extend to mesophilic strains. This study provides axenic culture evidence that atmospheric CO supports bacterial persistence and reports the third phylum, following Actinobacteria and Acidobacteria, to be experimentally shown to mediate the biogeochemically and ecologically important process of atmospheric H2 oxidation. This adds to the growing body of evidence that atmospheric trace gases are dependable energy sources for bacterial persistence.

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Section: Resultssupporting

confidence: 89%

Section: Resultsmentioning

confidence: 99%

Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

et al. 2019

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“…4). Carbohydrate metabolism was one of the most abundantly represented categories and has a key role in cell growth [42]. Expression of genes involved in most of the important steps in glycolysis was detected, and the expression of several glycolysis genes increased significantly in all three sediment samples during enrichment culturing (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Another way to enhance acetyl-CoA production was using the oxidative decarboxylation of pyruvate, which is generated from glycolysis, and the expression of genes related to the pyruvate dehydrogenase system was also significantly upregulated in the first stage (5 days) of enrichment. Acetyl-CoA is a molecule that participates in many biochemical reactions in protein, carbohydrate, and lipid metabolisms [42]. Its main function is to deliver the acetyl group to the TCA cycle to be oxidized for energy production.…”

Section: Resultsmentioning

confidence: 99%

Metatranscriptomic and comparative genomic insights into resuscitation mechanisms during enrichment culturing

et al. 2018

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BackgroundThe pure culture of prokaryotes remains essential to elucidating the role of these organisms. Scientists have reasoned that hard to cultivate microorganisms might grow in pure culture if provided with the chemical components of their natural environment. However, most microbial species in the biosphere that would otherwise be “culturable” may fail to grow because of their growth state in nature, such as dormancy. That means even if scientist would provide microorganisms with the natural environment, such dormant microorganisms probably still remain in a dormant state.ResultsWe constructed an enrichment culture system for high-efficiency isolation of uncultured strains from marine sediment. Degree of enrichment analysis, dormant and active taxa calculation, viable but non-culturable bacteria resuscitation analysis, combined with metatranscriptomic and comparative genomic analyses of the interactions between microbial communications during enrichment culture showed that the so-called enrichment method could culture the “uncultured” not only through enriching the abundance of “uncultured,” but also through the resuscitation mechanism. In addition, the enrichment culture was a complicated mixed culture system, which contains the competition, cooperation, or coordination among bacterial communities, compared with pure cultures.ConclusionsConsidering that cultivation techniques must evolve further—from axenic to mixed cultures—for us to fully understand the microbial world, we should redevelop an understanding of the classic enrichment culture method. Enrichment culture methods can be developed and used to construct a model for analyzing mixed cultures and exploring microbial dark matter. This study provides a new train of thought to mining marine microbial dark matter based on mixed cultures.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0613-2) contains supplementary material, which is available to authorized users.

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“…Assignment of protein functions to taxonomic groups is crucial when analyzing metabolic processes in microbial communities, since thousands of taxa contribute proteins with overlapping functions in an environmental sample. Increased abundance of some functions may thus be accompanied by decreased abundance of others in the same category, as shown to occur during exponential and stationary growth phases (34). We focused on the most abundant bacterial taxa to identify the metabolic particularities of organisms in P3 versus P2 (Fig.…”

Section: Discussionmentioning

confidence: 99%

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

Herlemann

Markert

Meeske

et al. 2019

Appl Environ Microbiol

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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.

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Comparative proteomics reveals signature metabolisms of exponentially growing and stationary phase marine bacteria

Cited by 31 publications

References 68 publications

Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

Metatranscriptomic and comparative genomic insights into resuscitation mechanisms during enrichment culturing

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

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