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The Genomic Basis of Trophic Strategy in Marine Bacteria

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The Genomic Basis of Trophic Strategy in Marine Bacteria The genomic basis of trophic strategy FEATURE ARTICLE in marine bacteria Federico M. Lauroa,b, Diane McDougaldc,1, Torsten Thomasc,1,Timothy J. Williamsb, Suhelen Eganb, Scott Ricec, Matthew Z. DeMaereb, Lily Tingb, Haluk Ertanb,d, Justin Johnsone, Steven Ferrierae, Alla Lapidusf, Iain Andersonf, Nikos Kyrpidesf, A. Christine Munkf, Chris Detterg, Cliff S. Hang, Mark V. Browna,b, Frank T. Robbh, Staffan Kjelleberga,c, and Ricardo Cavicchiolia,b,2 a b c Environmental Microbiology Initiative, School of Biotechnology and Biomolecular Sciences, and Centre for Marine Bio-Innovation, University of New SEE COMMENTARY South Wales, Sydney NSW 2052, Australia; eJ. Craig Venter Institute, 9704 Medical Center Drive, Rockville, MD 20850; fDepartment of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598; gDepartment of Energy Joint Genome Institute Bioscience Division, Los Alamos National Laboratory, Los Alamos, NM 87545; hCenter of Marine Biotechnology, University of Maryland Biotechnology Institute, Baltimore, MD 21202; and dDepartment of Molecular Biology and Genetics, Science Faculty, Istanbul University, Vezneciler, Istanbul 34118, Turkey This Feature Article is part of a series identified by the Editorial Board as reporting findings of exceptional significance. Edited by Rita R. Colwell, University of Maryland, College Park, MD, and approved July 28, 2009 (received for review March 30, 2009) Many marine bacteria have evolved to grow optimally at either among marine bacteria. However, although a large number of high (copiotrophic) or low (oligotrophic) nutrient concentrations, copiotrophic marine organisms (and fewer oligotrophs) have enabling different species to colonize distinct trophic habitats in been cultured, the study of trophic strategy has been impaired by the oceans. Here, we compare the genome sequences of two a lack of understanding of the molecular basis of adaptation. bacteria, Photobacterium angustum S14 and Sphingopyxis Here, we show that trophic strategy is strongly reflected in alaskensis RB2256, that serve as useful model organisms for copi- genomic content and genomic signatures can be used as a proxy otrophic and oligotrophic modes of life and specifically relate the for determining the ecological characteristics of uncultured genomic features to trophic strategy for these organisms and microorganisms, thereby allowing the assessment of trophic life SCIENCES define their molecular mechanisms of adaptation. We developed a strategies from bacterial genome sequences. model for predicting trophic lifestyle from genome sequence data ENVIRONMENTAL and tested >400,000 proteins representing >500 million nucleo- Results and Discussion tides of sequence data from 126 genome sequences with metage- Defining Genomic Signatures of Copiotrophs and Oligotrophs. We nome data of whole environmental samples. When applied to sequenced and annotated the genomes of two marine bacteria, available oceanic metagenome data (e.g., the Global Ocean Survey the copiotroph Photobacterium angustum S14 and the oligotroph data) the model demonstrated that oligotrophs, and not the more Sphingopyxis alaskensis RB2256, which are model representatives readily isolatable copiotrophs, dominate the ocean’s free-living of the two major classes of heterotrophic marine bacteria and for microbial populations. Using our model, it is now possible to define which extensive physiological data are available (Table 1). P. the types of bacteria that specific ocean niches are capable of angustum S14 was isolated from surface, coastal waters in Botany sustaining. Bay (Sydney), New South Wales, Australia (3). It is characterized Ͼ ␮ 3 ͉ ͉ by a relatively large cell size (growing cells 1 m ), and displays microbial adaptation and ecology microbial genomics and metagenomics a ‘‘feast and famine’’ strategy with rapid rates of growth (Ͼ1hϪ1) monitoring environmental health ͉ trophic adaptation in rich media and pronounced size reduction and other adaptive traits in response to nutrient limitation induced stasis. S. alasken- he marine environment is the largest habitat on Earth, account- sis RB2256 was isolated by extinction dilution as a numerically Ͼ Ϫ Ting for 90% of the biosphere by volume and harboring abundant member (Ͼ105 cells mL 1) of surface waters (10 m Ϸ microorganisms responsible for 50% of total global primary depth) in Resurrection Bay, Alaska and the North Sea, and a production. Within this environment, marine bacteria (and ar- closely related strain, AF01, was isolated from 350 m deep, chaea) play a pivotal role in biogeochemical cycles while constantly oligotrophic ocean waters near Japan (4–6). Oligotrophic traits assimilating, storing, transforming, exporting, and remineralizing of S. alaskensis include the ability to grow slowly with a constant the largest pool of organic carbon on the planet (1). maximum specific growth rate (Ͻ0.2 hϪ1) on low concentrations Nutrient levels in pelagic waters are not uniform. Large (nanomolar) of substrates and maintain a relatively small cell expanses of water are relatively nutrient depleted (e.g., oligo- volume (Ͻ0.1 ␮m3) and constant cell size in the shift between trophic open ocean water), whereas other zones are relatively starvation and growth conditions (6). The small size provides a nutrient rich (e.g., copiotrophic coastal and estuarine waters). Local variations in nutrient content can occur because of phys- ical processes, including upwelling of nutrient rich deep waters Author contributions: F.M.L. and R.C. designed research; J.J., S.F., A.L., I.A., N.K., A.C.M., and or aeolian and riverine deposition, or biological processes such C.D. performed research; D.M., L.T., H.E., and F.T.R. contributed new reagents/analytic as phytoplankton blooms or aggregation of particulate organic tools; F.M.L., D.M., T.T., T.J.W., S.E., S.R., M.Z.D., L.T., H.E., M.V.B., S.K., and R.C. analyzed matter. In addition, heterogeneity in ocean waters is not limited data; and F.M.L., T.T., S.K., and R.C. wrote the paper. to gross differences in nutrient concentrations, but extends to The authors declare no conflict of interest. microscale patchiness that occurs throughout the continuum of This article is a PNAS Direct Submission. ocean nutrient concentrations (2). Freely available online through the PNAS open access option. In ecological terms, bacteria are generally defined as r- Data deposition: The sequences reported in this paper have been deposited in the GenBank strategists, having a small body, short generation time, and highly database (accession nos. AAOJ00000000 and CP000356–CP000357). dispersible offspring. Although this strategy is broadly true See Commentary on page 15519. compared with macroorganisms, bacteria have evolved a wide 1D.M. and T.T. contributed equally to this work. range of growth and survival strategies to maximize reproductive 2To whom correspondence should be addressed. E-mail: [email protected]. success. In particular, nutrient type and availability have pro- This article contains supporting information online at www.pnas.org/cgi/content/full/ vided strong selective pressure for defining lifestyle strategies 0903507106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0903507106 PNAS ͉ September 15, 2009 ͉ vol. 106 ͉ no. 37 ͉ 15527–15533 Downloaded by guest on September 30, 2021 Table 1. Physiological characteristics of the model copiotroph P. angustum S14 and oligotroph S. alaskensis RB2256 Physiological characteristic P. angustum S14 S. alaskensis RB2256 Trophic strategy Copiotroph Oligotroph Growth strategy Feast and famine Equilibrium Cell size Large (Ͼ1 ␮m3) Small (Ͻ0.1 ␮m3) Maximum growth rate Ͼ1hϪ1 Ͻ0.2 hϪ1 Growth rate dependence on media richness Yes No Starvation cross-protection to high levels of other stress Yes No inducing agents Growing cells inherently resistant to stress inducing agents No Yes Lag phase after starvation Yes No rpoS-dependent reductive cell division Yes No Consistent cell yield during nutrient limited growth No Yes Data are from reviews by Kjelleberg et al. (38) and Cavicchioli et al. (6). mechanism for avoidance of predation, and the high surface present in the cell (because higher levels of expression from area-to-volume ratio allows for efficient nutrient acquisition fewer genes could compensate for this). In fact, the metapro- through high-affinity, broad-specificity uptake systems that are teome of the Sargasso Sea is overrepresented in SAR11 peptides predicted to enable S. alaskensis to be able to achieve doubling involved in transport and periplasmic substrate binding (10). times typically observed for bacteria in oligotrophic waters (6, 7). However, oligotrophs do have a reduced variety. Copiotrophs Genomic markers derived from the comparison of the S. alasken- are therefore characterized by transporter diversification and sis and P. angustum genomes were expanded and validated by specialization (e.g., PTS), and oligotrophs are characterized by searching 32 additional genome sequences, representing (i) related transporter protein minimization. species of Vibrionaceae and Sphingomonadaceae,(ii) other known The relatively higher number of secreted proteins in copi- aquatic copiotrophs and oligotrophs, and (iii) marine bacteria with otrophs is consistent with the higher ectoenzymatic activity high or low rRNA operon copy numbers. A total of 43 genetic observed in particle attached (mainly copiotrophic) vs. free- markers were identified (Fig. S1 and Table 2) that accurately living (mainly oligotrophic) bacteria (11, 12). The genomic predict
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