- Email: [email protected]
Environmental Genomics: Exploring Ecological Sequence Space
Dispatch R499
in Caenorhabditis elegans. Genes Dev. 17, 187–200. 14. Govindan, J.A., Cheng, H., Harris, J.E., and Greenstein, D. (2006). Antagonistic G-protein signaling pathways in parallel to an MSP/Eph receptor pathway to regulate meiotic diapause in Caenorhabditis elegans. Curr. Biol. 16, 1257–1268. 15. Corrigan, C., Subramanian, R., and Miller, M.A. (2005). Eph and NMDA receptors control Ca2+/calmodulindependent protein kinase II activation
during C. elegans oocyte meiotic maturation. Development 132, 5225–5237. 16. Rose, K.L., Winfrey, V.P., Hoffman, L.H., Hall, D.H., Furuta, T., and Greenstein, D. (1997). The POU gene ceh-18 promotes gonadal sheath cell differentiation and function required for meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 192, 59–77. 17. Detwiler, M.R., Reuben, M., Li, X., Rogers, E., and Lin, R. (2001). Two zinc finger proteins, OMA-1 and OMA-2,
Environmental Genomics: Exploring Ecological Sequence Space The ability to extract and characterize genomic DNA fragments from mixed microbial assemblages is providing novel insights into the ecology, evolution, and metabolism of uncultured microorganisms in nature. Robert M. Morris In 1987 Carl Woese used 16S ribosomal (r)RNA gene sequences from cultured organisms to reconstruct evolutionary relationships among the three domains of life [1]. Since that time, the scope of molecular diversity studies has rapidly progressed from genes in cultured organisms to genomes in mixed communities. Because most Bacteria and Archaea have not been cultured [2], the majority of genomic and metabolic information about microorganisms has come from a relatively small number of cultured representatives. Environmental sequencing studies, however, provide access to a much larger reservoir of genomic and metabolic information. Studies of marine and terrestrial ecosystems have led to novel discoveries clarifying evolutionary relationships among Bacteria and illuminating the roles of microorganisms in nutrient cycles and energy fluxes [3–7]. Recently, the nearly complete assembly of the genome of an uncultured bacterium, Kuenenia stuttgartiensis, revealed unique metabolic adaptations associated with anaerobic ammonium oxidation (anammox) [8]. Future studies are likely to become the
dominant source of microbial sequence information linking the metabolic process of specific microorganisms with environmental processes. Although relatively few environmental genomic studies have been conducted, approximately 33% of published microbial sequence data available through the NCBI genome project is from environmental samples (Figure 1A). The majority of these data, approximately two thirds (w13109 base pairs), is from a single study of Sargasso Sea bacterioplankton [4]. Although species richness and genetic microdiversity limited attempts to assemble large genomic fragments from even the most abundant bacterioplankton, the authors identified 782 novel genes encoding proteins related to rhodopsin-like photoreceptors, or proteorhodopsins. Sequences related to proteorhodopsins have also been identified in representatives from two of the ocean’s most abundant and widely distributed bacterioplankton lineages [9,10]. While the ecological significance of proteorhodopsins is uncertain, biochemical and proteomic analyses suggest that they function as light-driven proton pumps in seawater [10,11].
are redundantly required for oocyte maturation in C. elegans. Dev. Cell 1, 187–199.
Waksman Institute and Department of Genetics, Rutgers University, 190 Frelinghuysen Road, Piscataway, New Jersey 08854, USA. E-mail: [email protected] DOI: 10.1016/j.cub.2006.06.006
In a comparative environmental genomic study of marine and terrestrial samples, Tringe et al. [5] sequenced 75 million base pairs (Mbp) of microbial DNA from three deep-sea whale fall carcasses and 100 Mbp from an agricultural soil sample. A gene-centric approach was used to compare gene content from marine and terrestrial communities [3–5]. Environment-specific differences were identified in functional genes associated with ion transport and in energy production. For example, operons containing transporters for organic osmolites and sodium ion exporters were enriched in marine (Sargasso Sea and whale fall) samples and operons containing genes for active potassium channeling were enriched in the soil sample. Microbial communities varied as well, with differences observed in genome sizes and phylogenetic composition. Although large numbers of uncharacterized genes were identified in all samples, species richness was highest in agricultural soils, which contained as many as 3000 ribotypes. Calculations of species richness in Sargasso Sea and agricultural soil samples indicated that sequence coverage was low, 1% and 17%, respectively. This is not surprising, given that there is extensive genetic microdiveristy in natural microbial populations [12]. In contrast, sequence coverage among cultured representatives may be as high as 25% (Figure 1B). Although not all sequenced genomes are of validly described species, an estimate based on 915 genomes that have been completed or are in progress, 3,600 type cultures of validly described
Current Biology Vol 16 No 13 R500
A
B Total (4.5x109 bp)
Agricultural soil (1.0%) Unsequenced sample (99.0%)
Marine (1.3x109 bp) Sargasso Sea (17.6%)
Cultured (3.0x109 bp)
Sargasso Sea (marine) Deep-sea methane seep (marine) Acid mine drainage (terrestrial) North Pacific Ocean (marine) Soil and whalefall (marine and terrestrial)
Unsequenced sample (82.4%)
Terrestrial (1.8x108 bp)
Venter et al., [4] Hallam et al., [6] Tyson et al., [3] DeLong et al., [7] Tringe et al., [5]
Cultures (25.4%)
Unsequenced cultures (74.6%)
Current Biology
Figure 1. Environmental genomics to date. (A) A survey of genomic and environmental genomic sequence data. (B) Estimates of % coverage in representative samples. Marine and terrestrial contributions were based on five published environmental sequencing studies, and cultured contributions were based on completed genomes and genomes in progress. Sequence contributions and % coverage estimates were calculated using 331 completed genomes, 584 unfinished genomes, sequenced DNA (in base pairs) and species richness of environmental samples, and the average size of a completed microbial genome (3.3 million base pairs).
from microbial communities in nature will likely increase in the near future. As community sequence data are collected, microbial communities can be further characterized using this information to determine global patterns of gene expression and protein content. Environmental proteomic studies of mixed communities have already taken advantage of microbial sequence data by focusing on proteins from less complex communities and by targeting proteins from abundant organisms [10,15,16]. Ultimately, ‘omic’ information can help link specific uncultured microorganisms present in the environment with the processes they mediate and the responsible organisms can be targeted for isolation and characterization under more controlled laboratory conditions. References
species, and an average genome size of 3.3 Mbp, suggests that a large fraction of cultured species have been sequenced. While rough approximations, these data highlight the magnitude of unexplored ecological sequence space and the potential for new discoveries which might lead to metabolic insights about the roles of microorganisms in environmental processes. By focusing on less diverse microbial communities, Tyson et al. [3] assembled two nearly complete genomes and three partial genomes from an acid mine drainage biofilm community, and Strous et al. [8] assembled 98% of an uncultured anammox bacterium from a bioreactor. Genomic analyses of partial genome assemblies identified complete metabolic pathways and provided insights into nutrient cycles and energy fluxes, including carbon and nitrogen fixation, anaerobic ammonium oxidation, and energy generation. The nearly complete genome sequence of K. stuttgartiensis, a representative from the uncultured anammox bacterial lineage within the Planctomycetes, clarified Planctomycete evolution and revealed candidate genes associate with novel features of
catabolism and lipid biosynthesis. Interestingly, closely related anammox bacteria have been detected in diverse marine and terrestrial environments. 16S rDNA sequences most closely related to K. stuttgartiensis and other anammox bacteria have been recovered from anoxic waters in the Black Sea [13] and the oxygen minim waters of the Benguela upwelling system [14]. Together with 15N tracer experiments, these data suggest that anammox bacteria play an important role in the removal of fixed inorganic nitrogen from the oceans and, as a result, may limit primary productivity in many regions. Environmental genomic insights into the metabolism of an uncultured anammox bacterium will help microbiologists and oceanographers better characterize the link between anammox and the ocean’s nitrogen cycle. The success of environmental sequencing studies depends largely on cost, complexity, and question. However, significant reductions in sequencing costs, advances in sequencing strategies, and insights into microbial metabolism gained through previous studies, suggest that the amount of sequence information
1. Woese, C.R. (1987). Bacterial evolution. Microbiol. Rev. 51, 221–271. 2. Rappe, M.S., and Giovannoni, S.J. (2003). The uncultured microbial majority. Annu. Rev. Microbiol. 57, 369–394. 3. Tyson, G.W., Chapman, J., Hugenholtz, P., Allen, E.E., Ram, R.J., Richardson, P.M., Solovyev, V.V., Rubin, E.M., Rokhsar, D.S., and Banfield, J.F. (2004). Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43. 4. Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., Wu, D., Paulsen, I., Nelson, K.E., Nelson, W., et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74. 5. Tringe, S.G., von Mering, C., Kobayashi, A., Salamov, A.A., Chen, K., Chang, H.W., Podar, M., Short, J.M., Mathur, E.J., Detter, J.C., et al. (2005). Comparative metagenomics of microbial communities. Science 308, 554–557. 6. Hallam, S.J., Putnam, N., Preston, C.M., Detter, J.C., Rokhsar, D., Richardson, P.M., and DeLong, E.F. (2004). Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457–1462. 7. DeLong, E.F., Preston, C.M., Mincer, T., Rich, V., Hallam, S.J., Frigaard, N.U., Martinez, A., Sullivan, M.B., Edwards, R., Brito, B.R., et al. (2006). Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311, 496–503. 8. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., Horn, M., Daims, H., Bartol-Mavel, D., Wincker, P., et al. (2006). Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790–794. 9. Beja, O., Aravind, L., Koonin, E.V., Suzuki, M.T., Hadd, A., Nguyen, L.P., Jovanovich, S.B., Gates, C.M., Feldman, R.A., Spudich, J.L., et al. (2000). Bacterial rhodopsin: evidence for a new
Dispatch R501
type of phototrophy in the sea. Science 289, 1902–1906. 10. Giovannoni, S.J., Bibbs, L., Cho, J.C., Stapels, M.D., Desiderio, R., Vergin, K.L., Rappe, M.S., Laney, S., Wilhelm, L.J., Tripp, H.J., et al. (2005). Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85. 11. Beja, O., Spudich, E.N., Spudich, J.L., Leclerc, M., and DeLong, E.F. (2001). Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789. 12. Thompson, J.R., Pacocha, S., Pharino, C., Klepac-Ceraj, V., Hunt, D.E., Benoit, J., Sarma-Rupavtarm, R., Distel, D.L., and Polz, M.F. (2005). Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–1313.
13. Kuypers, M.M., Sliekers, A.O., Lavik, G., Schmid, M., Jorgensen, B.B., Kuenen, J.G., Sinninghe Damste, J.S., Strous, M., and Jetten, M.S. (2003). Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608–611. 14. Kuypers, M.M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B.M., Amann, R., Jorgensen, B.B., and Jetten, M.S. (2005). Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102, 6478–6483. 15. Ram, R.J., VerBerkmoes, N.C., Thelen, M.P., Tyson, G.W., Baker, B.J., Blake, R.C., Shah, M., Hettich, R.L., and Banfield, J.F. (2005). Community
Imprinting: Seeing Food and Eating It A recent study has found that although, ordinarily, cuttlefish hatchlings prefer shrimp-like prey, when visually exposed to crabs in the first hours of day one, they later prefer crabs to shrimps. As the development of this preference occurs during a short sensitive phase, does not depend on food ingestion and is long lasting, it fulfils all the criteria for imprinting, a phenomenon more usually associated with vertebrates and social learning. Susan D. Healy Early experiences in life can have a major impact on an animal’s behaviour. Sometimes the impact occurs almost immediately, sometimes it persists for a lifetime. When these experiences are acquired within a specified period of time (the ‘sensitive period’), have no obvious immediate reinforcement and last for a long time, they are considered to constitute a special kind of learning known as imprinting. In a recent study by Darmaillacq et al. [1], three-day old cuttlefish were found to prefer crabs over shrimps as a result of being visually exposed to crabs in the first few hours after hatching. Although early experience of particular foods influences subsequent food choice in a range of animals, even in humans (for example [2]), previous studies have either examined preferences after animals had ingested the test food (for example [3]), or not looked for the existence of a sensitive period (for example [4]). In this new study [1], cuttlefish that had hatched during the previous night were exposed to
small Carcinus crabs for between 15 and 120 minutes, during which time none of the crabs was consumed. On day three, the first day in which the hatchlings were provided with food (they usually do not eat before this time), they were offered both shrimps and crabs. Although some shrimps were eaten, the overwhelming preference was for crabs. However, this preference was dependent on two aspects of the early exposure: only those hatchlings that saw crabs within two hours after sunrise on their first day preferred crabs, compared with hatchlings exposed at 4 hours, or later, after sunrise; and only hatchlings that were exposed for 2 hours to crabs had a preference for crabs. Those hatchlings exposed to crabs for 15–60 minutes exhibited the usual innate preference for shrimp-like prey [5]. These preferences persisted for seven days and following consumption of shrimp. This kind of non-exclusive preference — three-day old hatchlings will eat shrimps, they simply prefer crabs — has similarities with sexual imprinting, in which juvenile animals develop
proteomics of a natural microbial biofilm. Science 308, 1915–1920. 16. Stapels, M.E., Cho, J.C., Giovannoni, S.J., and Barofsky, D.F. (2004). Proteomic analysis of novel marine bacteria using MALDI and ESI mass spectrometry. J. Biomol. Tech. 15, 191–198.
Department of Microbiology, Cornell University, Ithaca, New York 14853, USA. E-mail: [email protected]
DOI: 10.1016/j.cub.2006.06.007
preferences for mates based on the appearance and behaviour of, often, family members [6]. Young birds raised by parents of foster species often later choose mates from the foster species (leading to poor, or no, reproductive success), although they will mate with individuals from their own species if that is the only option. The lengthy duration of the food imprinting effect is also similar, although not to quite the same extent (as far as we know) as the effect on mate choice, which occurs months after the imprinting has occurred. Precocial animals, like domestic chicks and cuttlefish, which are independent within hours of hatch or birth and which receive no posthatch parental care have two options for acquisition of information: bring it into the world with you (unlearned preferences for food, sexual partners and so on) or pick up the information as you go (trial and error learning). Imprinting allows something in between: a certain degree of flexibility in response, useful for learning information for which the timing is likely to be predictable — food seen in first few hours of life, sibling/parents seen during juvenile stages — but in which specifying the exact details of the experience is not useful. Although food imprinting has previously attracted little attention, it seems that for animals such as cuttlefish there are clear advantages to learning the visual features of potential food items so as to deal with a world that is not filled with shrimp-like possibilities. What is less clear is
in Caenorhabditis elegans. Genes Dev. 17, 187–200. 14. Govindan, J.A., Cheng, H., Harris, J.E., and Greenstein, D. (2006). Antagonistic G-protein signaling pathways in parallel to an MSP/Eph receptor pathway to regulate meiotic diapause in Caenorhabditis elegans. Curr. Biol. 16, 1257–1268. 15. Corrigan, C., Subramanian, R., and Miller, M.A. (2005). Eph and NMDA receptors control Ca2+/calmodulindependent protein kinase II activation
during C. elegans oocyte meiotic maturation. Development 132, 5225–5237. 16. Rose, K.L., Winfrey, V.P., Hoffman, L.H., Hall, D.H., Furuta, T., and Greenstein, D. (1997). The POU gene ceh-18 promotes gonadal sheath cell differentiation and function required for meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 192, 59–77. 17. Detwiler, M.R., Reuben, M., Li, X., Rogers, E., and Lin, R. (2001). Two zinc finger proteins, OMA-1 and OMA-2,
Environmental Genomics: Exploring Ecological Sequence Space The ability to extract and characterize genomic DNA fragments from mixed microbial assemblages is providing novel insights into the ecology, evolution, and metabolism of uncultured microorganisms in nature. Robert M. Morris In 1987 Carl Woese used 16S ribosomal (r)RNA gene sequences from cultured organisms to reconstruct evolutionary relationships among the three domains of life [1]. Since that time, the scope of molecular diversity studies has rapidly progressed from genes in cultured organisms to genomes in mixed communities. Because most Bacteria and Archaea have not been cultured [2], the majority of genomic and metabolic information about microorganisms has come from a relatively small number of cultured representatives. Environmental sequencing studies, however, provide access to a much larger reservoir of genomic and metabolic information. Studies of marine and terrestrial ecosystems have led to novel discoveries clarifying evolutionary relationships among Bacteria and illuminating the roles of microorganisms in nutrient cycles and energy fluxes [3–7]. Recently, the nearly complete assembly of the genome of an uncultured bacterium, Kuenenia stuttgartiensis, revealed unique metabolic adaptations associated with anaerobic ammonium oxidation (anammox) [8]. Future studies are likely to become the
dominant source of microbial sequence information linking the metabolic process of specific microorganisms with environmental processes. Although relatively few environmental genomic studies have been conducted, approximately 33% of published microbial sequence data available through the NCBI genome project is from environmental samples (Figure 1A). The majority of these data, approximately two thirds (w13109 base pairs), is from a single study of Sargasso Sea bacterioplankton [4]. Although species richness and genetic microdiversity limited attempts to assemble large genomic fragments from even the most abundant bacterioplankton, the authors identified 782 novel genes encoding proteins related to rhodopsin-like photoreceptors, or proteorhodopsins. Sequences related to proteorhodopsins have also been identified in representatives from two of the ocean’s most abundant and widely distributed bacterioplankton lineages [9,10]. While the ecological significance of proteorhodopsins is uncertain, biochemical and proteomic analyses suggest that they function as light-driven proton pumps in seawater [10,11].
are redundantly required for oocyte maturation in C. elegans. Dev. Cell 1, 187–199.
Waksman Institute and Department of Genetics, Rutgers University, 190 Frelinghuysen Road, Piscataway, New Jersey 08854, USA. E-mail: [email protected] DOI: 10.1016/j.cub.2006.06.006
In a comparative environmental genomic study of marine and terrestrial samples, Tringe et al. [5] sequenced 75 million base pairs (Mbp) of microbial DNA from three deep-sea whale fall carcasses and 100 Mbp from an agricultural soil sample. A gene-centric approach was used to compare gene content from marine and terrestrial communities [3–5]. Environment-specific differences were identified in functional genes associated with ion transport and in energy production. For example, operons containing transporters for organic osmolites and sodium ion exporters were enriched in marine (Sargasso Sea and whale fall) samples and operons containing genes for active potassium channeling were enriched in the soil sample. Microbial communities varied as well, with differences observed in genome sizes and phylogenetic composition. Although large numbers of uncharacterized genes were identified in all samples, species richness was highest in agricultural soils, which contained as many as 3000 ribotypes. Calculations of species richness in Sargasso Sea and agricultural soil samples indicated that sequence coverage was low, 1% and 17%, respectively. This is not surprising, given that there is extensive genetic microdiveristy in natural microbial populations [12]. In contrast, sequence coverage among cultured representatives may be as high as 25% (Figure 1B). Although not all sequenced genomes are of validly described species, an estimate based on 915 genomes that have been completed or are in progress, 3,600 type cultures of validly described
Current Biology Vol 16 No 13 R500
A
B Total (4.5x109 bp)
Agricultural soil (1.0%) Unsequenced sample (99.0%)
Marine (1.3x109 bp) Sargasso Sea (17.6%)
Cultured (3.0x109 bp)
Sargasso Sea (marine) Deep-sea methane seep (marine) Acid mine drainage (terrestrial) North Pacific Ocean (marine) Soil and whalefall (marine and terrestrial)
Unsequenced sample (82.4%)
Terrestrial (1.8x108 bp)
Venter et al., [4] Hallam et al., [6] Tyson et al., [3] DeLong et al., [7] Tringe et al., [5]
Cultures (25.4%)
Unsequenced cultures (74.6%)
Current Biology
Figure 1. Environmental genomics to date. (A) A survey of genomic and environmental genomic sequence data. (B) Estimates of % coverage in representative samples. Marine and terrestrial contributions were based on five published environmental sequencing studies, and cultured contributions were based on completed genomes and genomes in progress. Sequence contributions and % coverage estimates were calculated using 331 completed genomes, 584 unfinished genomes, sequenced DNA (in base pairs) and species richness of environmental samples, and the average size of a completed microbial genome (3.3 million base pairs).
from microbial communities in nature will likely increase in the near future. As community sequence data are collected, microbial communities can be further characterized using this information to determine global patterns of gene expression and protein content. Environmental proteomic studies of mixed communities have already taken advantage of microbial sequence data by focusing on proteins from less complex communities and by targeting proteins from abundant organisms [10,15,16]. Ultimately, ‘omic’ information can help link specific uncultured microorganisms present in the environment with the processes they mediate and the responsible organisms can be targeted for isolation and characterization under more controlled laboratory conditions. References
species, and an average genome size of 3.3 Mbp, suggests that a large fraction of cultured species have been sequenced. While rough approximations, these data highlight the magnitude of unexplored ecological sequence space and the potential for new discoveries which might lead to metabolic insights about the roles of microorganisms in environmental processes. By focusing on less diverse microbial communities, Tyson et al. [3] assembled two nearly complete genomes and three partial genomes from an acid mine drainage biofilm community, and Strous et al. [8] assembled 98% of an uncultured anammox bacterium from a bioreactor. Genomic analyses of partial genome assemblies identified complete metabolic pathways and provided insights into nutrient cycles and energy fluxes, including carbon and nitrogen fixation, anaerobic ammonium oxidation, and energy generation. The nearly complete genome sequence of K. stuttgartiensis, a representative from the uncultured anammox bacterial lineage within the Planctomycetes, clarified Planctomycete evolution and revealed candidate genes associate with novel features of
catabolism and lipid biosynthesis. Interestingly, closely related anammox bacteria have been detected in diverse marine and terrestrial environments. 16S rDNA sequences most closely related to K. stuttgartiensis and other anammox bacteria have been recovered from anoxic waters in the Black Sea [13] and the oxygen minim waters of the Benguela upwelling system [14]. Together with 15N tracer experiments, these data suggest that anammox bacteria play an important role in the removal of fixed inorganic nitrogen from the oceans and, as a result, may limit primary productivity in many regions. Environmental genomic insights into the metabolism of an uncultured anammox bacterium will help microbiologists and oceanographers better characterize the link between anammox and the ocean’s nitrogen cycle. The success of environmental sequencing studies depends largely on cost, complexity, and question. However, significant reductions in sequencing costs, advances in sequencing strategies, and insights into microbial metabolism gained through previous studies, suggest that the amount of sequence information
1. Woese, C.R. (1987). Bacterial evolution. Microbiol. Rev. 51, 221–271. 2. Rappe, M.S., and Giovannoni, S.J. (2003). The uncultured microbial majority. Annu. Rev. Microbiol. 57, 369–394. 3. Tyson, G.W., Chapman, J., Hugenholtz, P., Allen, E.E., Ram, R.J., Richardson, P.M., Solovyev, V.V., Rubin, E.M., Rokhsar, D.S., and Banfield, J.F. (2004). Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43. 4. Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., Wu, D., Paulsen, I., Nelson, K.E., Nelson, W., et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74. 5. Tringe, S.G., von Mering, C., Kobayashi, A., Salamov, A.A., Chen, K., Chang, H.W., Podar, M., Short, J.M., Mathur, E.J., Detter, J.C., et al. (2005). Comparative metagenomics of microbial communities. Science 308, 554–557. 6. Hallam, S.J., Putnam, N., Preston, C.M., Detter, J.C., Rokhsar, D., Richardson, P.M., and DeLong, E.F. (2004). Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457–1462. 7. DeLong, E.F., Preston, C.M., Mincer, T., Rich, V., Hallam, S.J., Frigaard, N.U., Martinez, A., Sullivan, M.B., Edwards, R., Brito, B.R., et al. (2006). Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311, 496–503. 8. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., Horn, M., Daims, H., Bartol-Mavel, D., Wincker, P., et al. (2006). Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790–794. 9. Beja, O., Aravind, L., Koonin, E.V., Suzuki, M.T., Hadd, A., Nguyen, L.P., Jovanovich, S.B., Gates, C.M., Feldman, R.A., Spudich, J.L., et al. (2000). Bacterial rhodopsin: evidence for a new
Dispatch R501
type of phototrophy in the sea. Science 289, 1902–1906. 10. Giovannoni, S.J., Bibbs, L., Cho, J.C., Stapels, M.D., Desiderio, R., Vergin, K.L., Rappe, M.S., Laney, S., Wilhelm, L.J., Tripp, H.J., et al. (2005). Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85. 11. Beja, O., Spudich, E.N., Spudich, J.L., Leclerc, M., and DeLong, E.F. (2001). Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789. 12. Thompson, J.R., Pacocha, S., Pharino, C., Klepac-Ceraj, V., Hunt, D.E., Benoit, J., Sarma-Rupavtarm, R., Distel, D.L., and Polz, M.F. (2005). Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–1313.
13. Kuypers, M.M., Sliekers, A.O., Lavik, G., Schmid, M., Jorgensen, B.B., Kuenen, J.G., Sinninghe Damste, J.S., Strous, M., and Jetten, M.S. (2003). Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608–611. 14. Kuypers, M.M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B.M., Amann, R., Jorgensen, B.B., and Jetten, M.S. (2005). Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102, 6478–6483. 15. Ram, R.J., VerBerkmoes, N.C., Thelen, M.P., Tyson, G.W., Baker, B.J., Blake, R.C., Shah, M., Hettich, R.L., and Banfield, J.F. (2005). Community
Imprinting: Seeing Food and Eating It A recent study has found that although, ordinarily, cuttlefish hatchlings prefer shrimp-like prey, when visually exposed to crabs in the first hours of day one, they later prefer crabs to shrimps. As the development of this preference occurs during a short sensitive phase, does not depend on food ingestion and is long lasting, it fulfils all the criteria for imprinting, a phenomenon more usually associated with vertebrates and social learning. Susan D. Healy Early experiences in life can have a major impact on an animal’s behaviour. Sometimes the impact occurs almost immediately, sometimes it persists for a lifetime. When these experiences are acquired within a specified period of time (the ‘sensitive period’), have no obvious immediate reinforcement and last for a long time, they are considered to constitute a special kind of learning known as imprinting. In a recent study by Darmaillacq et al. [1], three-day old cuttlefish were found to prefer crabs over shrimps as a result of being visually exposed to crabs in the first few hours after hatching. Although early experience of particular foods influences subsequent food choice in a range of animals, even in humans (for example [2]), previous studies have either examined preferences after animals had ingested the test food (for example [3]), or not looked for the existence of a sensitive period (for example [4]). In this new study [1], cuttlefish that had hatched during the previous night were exposed to
small Carcinus crabs for between 15 and 120 minutes, during which time none of the crabs was consumed. On day three, the first day in which the hatchlings were provided with food (they usually do not eat before this time), they were offered both shrimps and crabs. Although some shrimps were eaten, the overwhelming preference was for crabs. However, this preference was dependent on two aspects of the early exposure: only those hatchlings that saw crabs within two hours after sunrise on their first day preferred crabs, compared with hatchlings exposed at 4 hours, or later, after sunrise; and only hatchlings that were exposed for 2 hours to crabs had a preference for crabs. Those hatchlings exposed to crabs for 15–60 minutes exhibited the usual innate preference for shrimp-like prey [5]. These preferences persisted for seven days and following consumption of shrimp. This kind of non-exclusive preference — three-day old hatchlings will eat shrimps, they simply prefer crabs — has similarities with sexual imprinting, in which juvenile animals develop
proteomics of a natural microbial biofilm. Science 308, 1915–1920. 16. Stapels, M.E., Cho, J.C., Giovannoni, S.J., and Barofsky, D.F. (2004). Proteomic analysis of novel marine bacteria using MALDI and ESI mass spectrometry. J. Biomol. Tech. 15, 191–198.
Department of Microbiology, Cornell University, Ithaca, New York 14853, USA. E-mail: [email protected]
DOI: 10.1016/j.cub.2006.06.007
preferences for mates based on the appearance and behaviour of, often, family members [6]. Young birds raised by parents of foster species often later choose mates from the foster species (leading to poor, or no, reproductive success), although they will mate with individuals from their own species if that is the only option. The lengthy duration of the food imprinting effect is also similar, although not to quite the same extent (as far as we know) as the effect on mate choice, which occurs months after the imprinting has occurred. Precocial animals, like domestic chicks and cuttlefish, which are independent within hours of hatch or birth and which receive no posthatch parental care have two options for acquisition of information: bring it into the world with you (unlearned preferences for food, sexual partners and so on) or pick up the information as you go (trial and error learning). Imprinting allows something in between: a certain degree of flexibility in response, useful for learning information for which the timing is likely to be predictable — food seen in first few hours of life, sibling/parents seen during juvenile stages — but in which specifying the exact details of the experience is not useful. Although food imprinting has previously attracted little attention, it seems that for animals such as cuttlefish there are clear advantages to learning the visual features of potential food items so as to deal with a world that is not filled with shrimp-like possibilities. What is less clear is