Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages

Ottesen, Elizabeth A.; Young, Charles W.; Gifford, Scott M.; Eppley, John M.; Marin, Roman; Schuster, Stephan C.; Scholin, Christopher A.; DeLong, Edward F.

doi:10.1126/science.1252476

Cited by 225 publications

(248 citation statements)

References 33 publications

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“…Owing to the multitude of possible local events in the highly dynamic North Sea (Sperling et al, 2012), a much higher spatial and temporal sampling resolution is required to cover the natural variability of both DOM and microbial community composition to an extent sufficient for revealing general trends of prevailing DOM-microbe interactions. The rapid response of microbial communities to such changing conditions was recently demonstrated by Ottesen et al (2014).…”

Section: Identifying the Key Factors-bcmentioning

confidence: 99%

“…The 'species' level provided the highest canonical correlations for the DNA/DOM and the RNA/DOM analyses, which is a promising basis for further in-depth studies to elucidate functional and mechanistic relationships between these features. Transcriptomic or proteomic analyses of individual bacteria and communities (Teeling et al, 2012;Ottesen et al, 2014) alongside the identification of DOM compounds in the exometabolome (Romano et al, 2014;Schwedt et al, 2015) and marine DOM, prospectively on a structural level, are most suitable approaches for such investigations.…”

Section: Identifying the Key Factors-bcmentioning

confidence: 99%

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Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system

et al. 2016

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Dissolved organic matter (DOM) is the main substrate and energy source for heterotrophic bacterioplankton. To understand the interactions between DOM and the bacterial community (BC), it is important to identify the key factors on both sides in detail, chemically distinct moieties in DOM and the various bacterial taxa. Next-generation sequencing facilitates the classification of millions of reads of environmental DNA and RNA amplicons and ultrahigh-resolution mass spectrometry yields up to 10 000 DOM molecular formulae in a marine water sample. Linking this detailed biological and chemical information is a crucial first step toward a mechanistic understanding of the role of microorganisms in the marine carbon cycle. In this study, we interpreted the complex microbiological and molecular information via a novel combination of multivariate statistics. We were able to reveal distinct relationships between the key factors of organic matter cycling along a latitudinal transect across the North Sea. Total BC and DOM composition were mainly driven by mixing of distinct water masses and presumably retain their respective terrigenous imprint on similar timescales on their way through the North Sea. The active microbial community, however, was rather influenced by local events and correlated with specific DOM molecular formulae indicative of compounds that are easily degradable. These trends were most pronounced on the highest resolved level, that is, operationally defined 'species', reflecting the functional diversity of microorganisms at high taxonomic resolution.

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Section: Identifying the Key Factors-bcmentioning

confidence: 99%

Section: Identifying the Key Factors-bcmentioning

confidence: 99%

Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system

et al. 2016

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“…On average, toward the ocean surface Prochlorococcus cells divide once a day (Vaulot et al, 1995), yet loss processes, for example by predation by grazers or infection by phage keep the total number of cells more-or-less stable (DuRand et al, 2001;Worden and Binder, 2003;Malmstrom et al, 2010;Ribalet et al, 2015). Carbon released through such interactions, as well as by excretion from living cells, likely provides a sizable fraction of the reduced carbon used for growth by co-occurring heterotrophic bacteria (Bertilsson et al, 2005;Ottesen et al, 2014;Biller et al, 2014b). Thus, like other phytoplankton, the life and death of Prochlorococcus are intimately coupled with that of co-occurring microbes.…”

Section: Introductionmentioning

confidence: 99%

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

Aharonovich

Sher

2016

The ISME Journal

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Interactions between marine microorganisms may determine the dynamics of microbial communities. Here, we show that two strains of the globally abundant marine cyanobacterium Prochlorococcus, MED4 and MIT9313, which belong to two different ecotypes, differ markedly in their response to coculture with a marine heterotrophic bacterium, Alteromonas macleodii strain HOT1A3. HOT1A3 enhanced the growth of MIT9313 at low cell densities, yet inhibited it at a higher concentration, whereas it had no effect on MED4 growth. The early transcriptomic responses of Prochlorococcus cells after 20 h in co-culture showed no evidence of nutrient starvation, whereas the expression of genes involved in photosynthesis, protein synthesis and stress responses typically decreased in MED4 and increased in MIT313. Differential expression of genes involved in outer membrane modification, efflux transporters and, in MIT9313, lanthipeptides (prochlorosins) suggests that Prochlorococcus mount a specific response to the presence of the heterotroph in the cultures. Intriguingly, many of the differentially-expressed genes encoded short proteins, including two new families of co-culture responsive genes: CCRG-1, which is found across the Prochlorococcus lineage and CCRG-2, which contains a sequence motif involved in the export of prochlorosins and other bacteriocin-like peptides, and are indeed released from the cells into the media.

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“…Such short-term fluctuations can have important ramifications for carbon and nutrient cycling (Ottesen et al, 2013). Further, information about how the relative abundances of uncultivated organisms vary over short time scales, particularly over the day-to-night cycle, could provide insight into their metabolic requirements and their relationship to other organisms (Ottesen et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem

et al. 2015

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Marine microbial communities experience daily fluctuations in light and temperature that can have important ramifications for carbon and nutrient cycling. Elucidation of such short time scale community-wide dynamics is hindered by system complexity. Hypersaline aquatic environments have lower species richness than marine environments and can be well-defined spatially, hence they provide a model system for diel cycle analysis. We conducted a 3-day time series experiment in a well-defined pool in hypersaline Lake Tyrrell, Australia. Microbial communities were tracked by combining cultivation-independent lipidomic, metagenomic and microscopy methods. The ratio of total bacterial to archaeal core lipids in the planktonic community increased by up to 58% during daylight hours and decreased by up to 32% overnight. However, total organism abundances remained relatively consistent over 3 days. Metagenomic analysis of the planktonic community composition, resolved at the genome level, showed dominance by Haloquadratum species and six uncultured members of the Halobacteriaceae. The post 0.8 μm filtrate contained six different nanohaloarchaeal types, three of which have not been identified previously, and cryo-transmission electron microscopy imaging confirmed the presence of small cells. Notably, these nano-sized archaea showed a strong diel cycle, with a pronounced increase in relative abundance over the night periods. We detected no eukaryotic algae or other photosynthetic primary producers, suggesting that carbon resources may derive from patchily distributed microbial mats at the sediment-water interface or from surrounding land. Results show the operation of a strong community-level diel cycle, probably driven by interconnected temperature, light abundance, dissolved oxygen concentration and nutrient flux effects.

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Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages

Cited by 225 publications

References 33 publications

Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system

Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem

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