Microbial community transcriptional networks are conserved in three domains at ocean basin scales

Aylward, Frank O.; Eppley, John M.; Smith, Jay W.; Chávez, Francisco P.; Scholin, Christopher A.; DeLong, Edward F.

doi:10.1073/pnas.1502883112

Cited by 168 publications

(190 citation statements)

References 34 publications

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“…Although some oligotrophs and copiotrophs may deviate from the overall pattern seen here, our conclusions were drawn from data on model taxa, most importantly, a SAR11 isolate, representing some of the most abundant bacteria in the ocean (7,8,22,23). The kinds of genetic controls used by oligotrophs have implications for understanding the networks of interactions among bacteria that appear to organize microbial communities (54). That the most abundant bacteria use alternatives to transcriptional control complicates the use of metatranscriptomic analyses to assess microbial activities in the ocean.…”

Section: Fig 4 Rank Abundance Of (A) Pelagibacter (B) Gammaproteobacmentioning

confidence: 75%

Transcriptional Control in Marine Copiotrophic and Oligotrophic Bacteria with Streamlined Genomes

Cottrell

Kirchman

2016

Appl Environ Microbiol

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Bacteria often respond to environmental stimuli using transcriptional control, but this may not be the case for marine bacteria such as "Candidatus Pelagibacter ubique," a cultivated representative of the SAR11 clade, the most abundant organism in the ocean. This bacterium has a small, streamlined genome and an unusually low number of transcriptional regulators, suggesting that transcriptional control is low in Pelagibacter and limits its response to environmental conditions. Transcriptome sequencing during batch culture growth revealed that only 0.1% of protein-encoding genes appear to be under transcriptional control in Pelagibacter and in another oligotroph (SAR92) whereas >10% of genes were under transcriptional control in the copiotrophs Polaribacter sp. strain MED152 and Ruegeria pomeroyi. When growth levels changed, transcript levels remained steady in Pelagibacter and SAR92 but shifted in MED152 and R. pomeroyi. Transcript abundances per cell, determined using an internal RNA sequencing standard, were low (<1 transcript per cell) for all but a few of the most highly transcribed genes in all four taxa, and there was no correlation between transcript abundances per cell and shifts in the levels of transcription. These results suggest that low transcriptional control contributes to the success of Pelagibacter and possibly other oligotrophic microbes that dominate microbial communities in the oceans. IMPORTANCEDiverse heterotrophic bacteria drive biogeochemical cycling in the ocean. The most abundant types of marine bacteria are oligotrophs with small, streamlined genomes. The metabolic controls that regulate the response of oligotrophic bacteria to environmental conditions remain unclear. Our results reveal that transcriptional control is lower in marine oligotrophic bacteria than in marine copiotrophic bacteria. Although responses of bacteria to environmental conditions are commonly regulated at the level of transcription, metabolism in the most abundant bacteria in the ocean appears to be regulated by other mechanisms.

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Section: Fig 4 Rank Abundance Of (A) Pelagibacter (B) Gammaproteobacmentioning

confidence: 75%

Transcriptional Control in Marine Copiotrophic and Oligotrophic Bacteria with Streamlined Genomes

Cottrell

Kirchman

2016

Appl Environ Microbiol

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“…Nevertheless, detailed analyses of the same data set showed pronounced peaks in expression of the glyoxylate shunt gene encoding isocitrate lyase in the tricarboxylic acid (TCA) cycle coinciding with highest solar irradiance, which were suggested to be tightly linked to PR phototrophy (117). Even more pronounced diurnal dynamics in isocitrate lyase gene expression in a wide variety of Proteobacteria clades (e.g., SAR11 and SAR86) were then found using automated sampling in both California coastal waters and the North Pacific Subtropical Gyre (118). Using the same automated sampler, with sampling extended over 3 days at station ALOHA, pronounced diurnal cycles in gene expression patterns of both photoautotrophs and photoheterotrophs (including both PR-and bacteriochlorophyll-containing bacteria) were observed (119).…”

Section: Environmental Rhodopsin Gene Expression Analysesmentioning

confidence: 84%

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Pinhassi

DeLong

Béjà

et al. 2016

Microbiol Mol Biol Rev

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175

172

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SUMMARYThe recognition of a new family of rhodopsins in marine planktonic bacteria, proton-pumping proteorhodopsin, expanded the known phylogenetic range, environmental distribution, and sequence diversity of retinylidene photoproteins. At the time of this discovery, microbial ion-pumping rhodopsins were known solely in haloarchaea inhabiting extreme hypersaline environments. Shortly thereafter, proteorhodopsins and other light-activated energy-generating rhodopsins were recognized to be widespread among marine bacteria. The ubiquity of marine rhodopsin photosystems now challenges prior understanding of the nature and contributions of “heterotrophic” bacteria to biogeochemical carbon cycling and energy fluxes. Subsequent investigations have focused on the biophysics and biochemistry of these novel microbial rhodopsins, their distribution across the tree of life, evolutionary trajectories, and functional expression in nature. Later discoveries included the identification of proteorhodopsin genes in all three domains of life, the spectral tuning of rhodopsin variants to wavelengths prevailing in the sea, variable light-activated ion-pumping specificities among bacterial rhodopsin variants, and the widespread lateral gene transfer of biosynthetic genes for bacterial rhodopsins and their associated photopigments. Heterologous expression experiments with marine rhodopsin genes (and associated retinal chromophore genes) provided early evidence that light energy harvested by rhodopsins could be harnessed to provide biochemical energy. Importantly, some studies with native marine bacteria show that rhodopsin-containing bacteria use light to enhance growth or promote survival during starvation. We infer from the distribution of rhodopsin genes in diverse genomic contexts that different marine bacteria probably use rhodopsins to support light-dependent fitness strategies somewhere between these two extremes.

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“…These bacteria are generally heterotrophs, able to metabolize a variety of labile and recalcitrant organic substrates, including monocyclic and polycyclic aromatic hydrocarbons as well as various algal osmolytes and other metabolites (173,175,272,594,(762)(763)(764)(765)(766)(767). They usually react to and grow quickly after small increases in levels of labile organic substrates, such as amino acids, simple sugars, and DMSP, especially during the initial phase of algal blooms (8,13,252,265,272,(768)(769)(770)(771)(772).…”

Section: The Marine Roseobacter Cladementioning

confidence: 99%

Microbial Surface Colonization and Biofilm Development in Marine Environments

Dang

Lovell

2016

Microbiol Mol Biol Rev

870

636

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SUMMARYBiotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.

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Microbial community transcriptional networks are conserved in three domains at ocean basin scales

Cited by 168 publications

References 34 publications

Transcriptional Control in Marine Copiotrophic and Oligotrophic Bacteria with Streamlined Genomes

Transcriptional Control in Marine Copiotrophic and Oligotrophic Bacteria with Streamlined Genomes

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Microbial Surface Colonization and Biofilm Development in Marine Environments

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