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Home , Paradox of the plankton

COMMENTARY

The trophic tapestry of the sea

Matthew J. Church1 Department of Oceanography, University of Hawaii, 1000 Pope Road, Honolulu, HI 96822

ceanic are the as a powerful proxy for defining micro- largest on Earth, bial lifestyles. and living in these systems is dominated by Location, Location, Location Oplanktonic . Microbial To the casual observer ocean ecosys- ecologists have long sought to under- tems may appear relatively homogenous; stand the role of environmental in reality, these environments are ripe selection in shaping the diversity of with heterogeneity. Climate forc- planktonic microorganisms. The oceans ing of ocean currents, wind-driven mix- have proven a dauntingly complex arena ing, stratification, and all can to conduct such studies. Marine ecosys- contribute to seascape variability (7). tems are immense and remote and Moreover, numerous biotic processes hence chronically undersampled. More- result in patchy distributions. over, the enormous diversity of plank- Dead or decaying cells, excre- tonic microorganisms challenges our ment, and spillage of cellular contents most sophisticated computational capa- into seawater by grazing or viral lysis all bilities. Only recently, through creative can form transient ‘‘hot spots’’ of nutri- applications of new technologies have ents and energy substrates against an oceanographers begun to overcome some Fig. 1. Representation of the ocean as a microbial otherwise dilute resource pool (8, 9). habitat; vertical gradients in sunlight are superim- of these hurdles. In this issue of PNAS, Singularly or together these processes Lauro et al. (1) use a comparative ge- posed on depth-dependent changes in inorganic nutrient concentrations (black line). The majority introduce habitat heterogeneity to the nome approach to provide insight into of bacteria (vertical changes in de- ocean. The rich extant of how environmental pressures have shaped picted by red line) exist as members of the free- oceanic plankton suggest marine micro- lifestyles. The study high- living plankton (shown in white). These abundant organisms exploit this heterogeneity, lights key differences in the genomes of are found throughout low-nutrient effectively partitioning oceanic resources two oceanic bacteria: Sphingopyxis ocean ecosystems. Other groups of microorgan- into countless ecological niches. alaskensis, an abundant ␣-proteobacterium isms (shown in yellow) appear specially adapted to use nutrient-enriched microhabitats enriched in Such habitat complexity can be over- adapted to low-nutrient oceanic environ- lain against a highly structured resource ments, and Photobacterium angustum,a organic nutrients such as those depicted by the field. For example, strong vertical gradi- ␥-proteobacterium that grows optimally colonized organic matter aggregate. ents in sunlight and bioessential nutri- in nutrient-enriched seawater. By exam- ents define upper ocean ecosystems, and ining the genetic underpinnings that dif- microorganisms capitalize on the niche ferentiate these microorganisms the study standing of how these communities space afforded by such gradients (5, 10, uses the lens of molecular biology to view evolve, what the forces are that collec- 11). In the thin skin of the upper ocean lifestyle features of ocean microbes. tively work to shape their biodiversity, and how this biodiversity is maintained where sunlight is bountiful, phototrophic Background remain issues at the forefront of micro- microorganisms capture light energy for Tiny (Ͻ2 ␮m in diameter), single-celled bial . synthesis of organic material. This pho- plankton are abundant in seawater and The article by Lauro et al. (1) serves tosynthetically produced organic matter comprise some of the largest inventories as an excellent example of how environ- fuels innumerable cellular metabolisms of biomass on the planet (2). Planktonic mental genomics can inform our within the ocean’s . However, communities contain representatives of understanding of the types of selective microbial life is notoriously leaky, and a all three domains of life (Bacteria, Ar- pressures driving bacterial evolution in major fraction of this organic matter chaea, and Eukarya), and these microor- nature. Through painstaking comparison solubilizes to dissolved constituents in seawater. This diffuse, but reactive, pool ganism assemblages catalyze a dizzying of genome features that differentiate S. of dissolved organic matter (DOM) array of services vital to the alaskensis from P. angustum, Lauro et serves as the primary food source for habitability of Earth. The biodiversity of al. identify 43 lifestyle-distinguishing ocean microbes is staggering; a typical diverse assemblages of heterotrophic genetic markers that they use to formu- prokaryotes. The vast majority of these liter of seawater contains billions of late a model to characterize the trophic cells and thousands of genetically dis- heterotrophic microbes exist as free- lifestyles of microorganisms. The result- tinct individuals. For decades aquatic living members of the plankton, and ing clustering of genome sequence space ecologists have sought to understand their utilization of DOM is a major how these planktonic communities sus- renders a remarkable tapestry of micro- component of the ocean’s carbon cycle tain such diversity (3–5). Ecological the- bial lifestyles. Time will tell whether this (12). An important consequence of pho- ory predicts that at equilibrium multiple model is sufficiently robust to predict tosynthetic cellular production is the competing for the same resource the tapestry’s topology at the increas- depletion of bioessential inorganic nutri- pools cannot stably coexist (6). How- ingly finer scales likely required for the ever, nucleic acid sequence information wave of metagenomic data emerging derived from ocean plankton indicates from the sea. Nonetheless, the model’s Author contributions: M.J.C. wrote the paper. these ecosystems are inhabited by some reproduction of phenotypic characteris- The author declares no conflict of interest. of the most diverse microorganism as- tics based on genetic clustering reaffirms See companion article on page 15527. semblages on the planet. Our under- that DNA sequence information serves 1E-mail: [email protected].

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0908881106 PNAS ͉ September 15, 2009 ͉ vol. 106 ͉ no. 37 ͉ 15519–15520 Downloaded by guest on September 29, 2021 ents throughout the well-lit regions of substrate concentrations (16). Overrep- genome sequences of Prochlorococcus the sea (Fig. 1). Major life-requiring resentation of lipid metabolism path- and SAR11 bacterial lineages (10). sources of inorganic nutrients (nitrogen, ways and low numbers of rRNA operons Ecotypic variation among these organ- phosphorus, iron) are often found at also appear characteristic of the oligo- isms appears to permit very closely re- vanishingly low concentrations in the trophic lifestyle (1), suggesting olig- lated relatives to coexist in distinct, non- upper ocean (7). The dilute pool of nu- otrophs value acquisition of energy at competitive ecological space (10, 11). trient resources promotes fierce compe- the expense of rapid growth (17). The In contrast to the majority olig- tition, resulting in tightly linked food small number and low diversity of sub- otrophs, copiotrophic microorganisms web dynamics. However, rapid turnover strate receptors reflects life as a gener- capitalize on the variable resource- in planktonic biomass also provides alist, capitalizing on the broad biochemi- enriched habitats in the sea. Copi- countless opportunities for fine-tuning cal complexity of ocean DOM pools. otrophs are large (Ͼ1 ␮m in diameter), of cellular processes through genetic Intriguing patterns have begun to grow rapidly (doubling times of hours), diversification. emerge from genome and metagenome carry relatively large genomes, and have evolved complex systems for sensing and Finding the Right Lifestyle responding to their environment (1). The comparative genome approach of DNA sequence Relaxed selective pressure to conserve Lauro et al. (1) demonstrates that gene gene content appears to have permitted content can reflect diversification information serves as a these organisms to evolve numerous and among microbial trophic strategies. On diverse, highly specialized substrate one end of the microbial lifestyle spec- powerful proxy for transport systems. Intriguingly, met- trum lie the oligotrophs, organisms spe- agenomic analyses of deep-sea micro- cifically adapted to life in low-nutrient defining microbial plankton suggest such characteristics environments; the other end holds the may typify microbial lifestyles in the , microbes specialized for lifestyles. cold, energy-starved habitats that domi- life in nutrient-enriched habitats of the nate the ocean’s interior (20). sea. Given the high demand for nutrient Aided by studies such as this one by and energy resources in the ocean it is sequences of Lauro et al. (1), ecologists are becoming not altogether surprising that many of that provide clues to many of the selec- empowered with tools to assimilate the the numerically dominant microbes tive pressures imposed on life in the sea. torrent of genome and metagenome se- found in seawater are adapted to growth Notably, many of the oceanic oligotrophs on dilute substrate pools. Isolates of appear to have reduced their gene con- quences emerging from the ocean. Sev- Pelagibacter ubique, strains of cyanobac- tent to conserve energy and nutrient eral striking patterns have already begun teria belonging to the genus Prochloro- demands associated with gene replica- to emerge: (i) the ocean harbors func- coccus, and metagenomic sequences tion, regulation, and repair (14, 18, 19). tionally diverse microorganisms; (ii) obtained from low-nutrient marine sys- However, it remains unclear how ge- gene content reflects strong environ- tems sampled by the Global Ocean Sur- nome streamlining impacts the breadth mental selective pressures; (iii) numeri- vey (13) all cluster in genome space of ecological space these organisms oc- cally dominant ocean microorganisms among oligotrophs (1). Oligobacteria cupy. The loss of specific biochemical minimize their genome size, with con- share several common features: they are pathways could result in finer and finer comitant biogeochemical and ecological extremely small (some Ͻ0.2 ␮mindi- partitioning of ocean niches, with associ- consequences; and (iv) the complex mi- ameter), grow very slowly (doubling ated loss of functional diversity. Alter- lieu of ocean resources favors flexible times of Ͼ1 day), and possess broad natively, genome streamlining could re- metabolic capabilities. Analyses such as specificity, but high-affinity substrate inforce those genetic pathways that those reported by Lauro et al. are indis- transport systems (14, 15). Such adapta- enable broader functional capacity, for pensable for testing hypotheses about tions enable these organisms to extract a example through mixotrophy, while re- the strategies microorganisms use to ac- wide spectrum of compound classes ducing redundant and nonessential quire resources and how such strategies from seawater (e.g., small peptides, lip- genes. Evidence for fine-scale partition- reflect selective pressures that collec- ids, simple sugars) even at very low ing of resources can be observed in the tively shape plankton biodiversity.

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15520 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0908881106 Church Downloaded by guest on September 29, 2021