Unsuspected diversity among marine aerobic anoxygenic phototrophs

Béjà, Oded; Suzuki, Marcelino T.; Heidelberg, John F.; Nelson, Karen E.; Preston, Christina M.; Hamada, Tohru; Eisen, Jonathan A.; Fraser, Claire M.; DeLong, Edward F.

doi:10.1038/415630a

Cited by 378 publications

(265 citation statements)

References 23 publications

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“…Recent studies suggest that AAPs constitute a considerable fraction of marine planktonic community, and may contribute significantly to the carbon cycle in the ocean via facultative photoheterotrophy (Kolber et al, 2001;Béjà et al, 2002). Living in an oligotrophic environment, oceanic AAPs likely are capable of efficiently controlling the expression of their photosynthetic apparatus, supplementing heterotrophic metabolism with light-dependent energy harvest.…”

Section: Microbial Metatranscriptomics In the Open Ocean Y Shi Et Almentioning

confidence: 99%

Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean

et al. 2010

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As part of an ongoing survey of microbial community gene expression in the ocean, we sequenced and compared B38 Mbp of community transcriptomes and B157 Mbp of community genomes from four bacterioplankton samples, along a defined depth profile at Station ALOHA in North Pacific subtropical gyre (NPSG). Taxonomic analysis suggested that the samples were dominated by three taxa: Prochlorales, Consistiales and Cenarchaeales, which comprised 36-69% and 29-63% of the annotated sequences in the four DNA and four cDNA libraries, respectively. The relative abundance of these taxonomic groups was sometimes very different in the DNA and cDNA libraries, suggesting differential relative transcriptional activities per cell. For example, the 125 m sample genomic library was dominated by Pelagibacter (B36% of sequence reads), which contributed fewer sequences to the community transcriptome (B11%). Functional characterization of highly expressed genes suggested taxon-specific contributions to specific biogeochemical processes. Examples included Roseobacter relatives involved in aerobic anoxygenic phototrophy at 75 m, and an unexpected contribution of low abundance Crenarchaea to ammonia oxidation at 125 m. Read recruitment using reference microbial genomes indicated depth-specific partitioning of coexisting microbial populations, highlighted by a transcriptionally active high-light-like Prochlorococcus population in the bottom of the photic zone. Additionally, nutrient-uptake genes dominated Pelagibacter transcripts, with apparent enrichment for certain transporter types (for example, the C4-dicarboxylate transport system) over others (for example, phosphate transporters). In total, the data support the utility of coupled DNA and cDNA analyses for describing taxonomic and functional attributes of microbial communities in their natural habitats.

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Section: Microbial Metatranscriptomics In the Open Ocean Y Shi Et Almentioning

confidence: 99%

Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean

et al. 2010

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“…HTCC2255 and Polaribacter. In recent years, a number of potential mechanisms by which light might influence the metabolism of heterotrophs in the ocean have been discovered (Béjà et al, 2000(Béjà et al, , 2002Kolber et al, 2001;Venter et al, 2004). Proteorhodopsin made up 0.18-0.82% of HTCC2255-like and 0.42-1.18% of Polaribacter-like transcripts.…”

Section: Percent Of Kegg-annotated Transcriptsmentioning

confidence: 99%

Metatranscriptomic analysis of autonomously collected and preserved marine bacterioplankton

et al. 2011

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Planktonic microbial activity and community structure is dynamic, and can change dramatically on time scales of hours to days. Yet for logistical reasons, this temporal scale is typically undersampled in the marine environment. In order to facilitate higher-resolution, long-term observation of microbial diversity and activity, we developed a protocol for automated collection and fixation of marine microbes using the Environmental Sample Processor (ESP) platform. The protocol applies a preservative (RNALater) to cells collected on filters, for long-term storage and preservation of total cellular RNA. Microbial samples preserved using this protocol yielded high-quality RNA after 30 days of storage at room temperature, or onboard the ESP at in situ temperatures. Pyrosequencing of complementary DNA libraries generated from ESP-collected and preserved samples yielded transcript abundance profiles nearly indistinguishable from those derived from conventionally treated replicate samples. To demonstrate the utility of the method, we used a moored ESP to remotely and autonomously collect Monterey Bay seawater for metatranscriptomic analysis. Community RNA was extracted and pyrosequenced from samples collected at four time points over the course of a single day. In all four samples, the oxygenic photoautotrophs were predominantly eukaryotic, while the bacterial community was dominated by Polaribacter-like Flavobacteria and a Rhodobacterales bacterium sharing high similarity with Rhodobacterales sp. HTCC2255. However, each time point was associated with distinct species abundance and gene transcript profiles. These laboratory and field tests confirmed that autonomous collection and preservation is a feasible and useful approach for characterizing the expressed genes and environmental responses of marine microbial communities.

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“…Heterotrophic marine microbes exhibit various levels of specialization for the uptake and processing of specific components of the dissolved organic matter pool (Pomeroy et al, 2007;Poretsky et al, 2010;Teeling et al, 2012). Moreover, recent studies have uncovered novel metabolic capabilities in marine bacteria and archaea, including rhodopsin-based phototrophy (Béjà et al, 2000), aerobic anoxygenic phototrophy (Béjà et al, 2002), CO 2 fixation (Newton et al, 2010) and chemolithotrophic oxidation of inorganic compounds such as ammonia (Walker et al, 2010), sulfur (Walsh et al, 2009) and hydrogen (Anantharaman et al, 2013). Metagenomics and single-cell amplified genomes have provided insight into the diversity and metabolic potential of microbial communities in the ocean (DeLong et al, 2006;Yooseph et al, 2007;Woyke et al, 2009;Swan et al, 2011;Grzymski et al, 2012;Rinke et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton

et al. 2014

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In this study, we used comparative metaproteomics to investigate the metabolic activity of microbial plankton inhabiting a seasonally hypoxic basin in the Northwest Atlantic Ocean (Bedford Basin). From winter to spring, we observed a seasonal increase in high-affinity membrane transport proteins involved in scavenging of organic substrates; Rhodobacterales transporters were strongly associated with the spring phytoplankton bloom, whereas SAR11 transporters were abundant in the underlying waters. A diverse array of transporters for organic compounds were similar to the SAR324 clade, revealing an active heterotrophic lifestyle in coastal waters. Proteins involved in methanol oxidation (from the OM43 clade) and carbon monoxide (from a wide variety of bacteria) were identified throughout Bedford Basin. Metabolic niche partitioning between the SUP05 and ARCTIC96BD-19 clades, which together comprise the Gamma-proteobacterial sulfur oxidizers group was apparent. ARCTIC96BD-19 proteins involved in the transport of organic compounds indicated that in productive coastal waters this lineage tends toward a heterotrophic metabolism. In contrast, the identification of sulfur oxidation proteins from SUP05 indicated the use of reduced sulfur as an energy source in hypoxic bottom water. We identified an abundance of Marine Group I Thaumarchaeota proteins in the hypoxic deep layer, including proteins for nitrification and carbon fixation. No transporters for organic compounds were detected among the thaumarchaeal proteins, suggesting a reliance on autotrophic carbon assimilation. In summary, our analyses revealed the spatiotemporal structure of numerous metabolic activities in the coastal ocean that are central to carbon, nitrogen and sulfur cycling in the sea.

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Unsuspected diversity among marine aerobic anoxygenic phototrophs

Cited by 378 publications

References 23 publications

Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean

Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean

Metatranscriptomic analysis of autonomously collected and preserved marine bacterioplankton

Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton

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