Recruitment in the sea: bacterial genes required for inducing larval settlement in a polychaete worm

Ying, Huang; Callahan, Sean M.; Hadfield, Michael G.

doi:10.1038/srep00228

Cited by 79 publications

(79 citation statements)

References 43 publications

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“…Larvae can be reared with the same algal culture, and will metamorphose within one week. For the same reasons, Hydroides is a choice model for studies of larval settlement and metamorphosis (Shikuma et al, 2014;Carpizio-Ituarte and Hadfield, 1998;Qian and Pechenik, 1998;Hadfield et al, 2001;Huang et al, 2012). Regeneration of the operculum and body after transversal sectioning has been reported, including anterior body regeneration (Zeleny, 1902), which is less prevalent in polychaetes (Bely, 2006).…”

Section: Experimental Advantages and Challengesmentioning

confidence: 99%

Development of a feeding trochophore in the polychaete Hydroides elegans

Arenas-Mena¹,

Li²

2014

Int. J. Dev. Biol.

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Hydroides elegans is an indirectly developing polychaete with equal spiral cleavage, gastrulation by invagination, and a feeding trochophore. Expression of several transcription factors and differentiation genes has been characterized. Comparative analysis reveals evolutionarily conserved roles. For example, the synexpression of transcription factors FoxA and Brachyury suggests homology of primary and secondary gut openings in protostomes and deuterostomes, and the expression of Sall suggests similar regulatory controls in the posterior growth zone of bilaterians. Differences in gene expression suggest regulatory differences control gastrulation by invagination in polychaetes with a feeding trochophore and gastrulation by epiboly in polychaetes without a feeding trochophore. Association of histone variant H2A.Z with transcriptional potency and its expression suggest a developmental role during both embryogenesis and the larva-to-adult transformation. Methods are being developed for experimental exploration of the gene regulatory networks involved in trochophore development in Hydroides. It is unknown if polychaete feeding trochophores evolved from a larval stage already present in the life cycle of the last common ancestor of protostomes and deuterostomes. Previous evolutionary scenarios about larval origins overemphasize the discontinuity between larval and adult development and require the early evolution of undifferentiated and transcriptionally potent "set aside" cells. Indirect development may proceed by developmental remodeling of differentiated cells and could have evolved after gradual transformation of juveniles into larvae; undifferentiated and transcriptionally potent cells would have evolved secondarily. Comprehensive characterization of gene regulatory networks for feeding trochophore development may help resolve these major evolutionary questions. KEY WORDS: bilaterian, posterior growth, serpulid, annelidHydroides elegans, a polychaete with a feeding trochophore Characterization of polychaetes with a feeding trochophore, such as Hydroides elegans ( Fig. 1 and Table 1), is relevant to understand the developmental evolution of complex life cycles in spiralians. Embryonic development in polychaetes conforms to the presence or absence of a feeding trochophore (Fig. 2). In the genus Hydroides (Eupomatus), embryogenesis ends in a feeding trochophore endowed with an equatorial ciliary band, a protonephridium, various sensory organs, and a functional gut formed after gastrulation by invagination (Hatschek, 1885;Shearer, 1911). Blastomeres 4d and 2d22 are inconspicuous and fated to contribute to the mesodermal and ectodermal portions of the segmented body that will have primarily a reproductive role; the Int. J. Dev. Biol. 58: 575-583 (2014) growth and proliferation of 4d and 2d22 are feeding-dependent. In contrast, during embryogenesis in polychaetes without feeding larvae, blastomeres 4d and 2d are relatively large and immediately engage in the formation of segments (Fig. 2). In addition to la...

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Section: Experimental Advantages and Challengesmentioning

confidence: 99%

Development of a feeding trochophore in the polychaete Hydroides elegans

Arenas-Mena¹,

Li²

2014

Int. J. Dev. Biol.

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“…Recent studies demonstrate that the larvae of many benthic marine invertebrates require specific microbial cues for their recruitment from the plankton, and these larval responses to bacteria influence the structuring of many marine benthic communities (60,107). For example, certain strains of the biofilm-forming bacterium Pseudoalteromonas luteoviolacea produce chemical cues that stimulate settlement and metamorphosis by Hydroides elegans, a polychaete worm that fouls docks and the hulls of ships worldwide (60,108), as well as a sea urchin (109) and a coral (107). Surface biofilms on many marine animals serve important functions in determining the very nature of the animals' ecological interactions with other organisms (110).…”

Section: Nested Ecosystemsmentioning

confidence: 99%

Animals in a bacterial world, a new imperative for the life sciences

McFall‐Ngai

Hadfield

Bosch

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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2,250

1,916

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In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal–bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other’s genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal–bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world

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“…The tasks involve choosing a new habitat to settle on, switching the molecular machinery to adapt to sessile life, and building a protective calcareous shell or tube by controlled calcification (Thiyagarajan, 2010). In recent years, rapid developments in environmental molecular biology and chemical ecology have shed light on some key questions: how do larvae choose where to settle (Huang et al, 2012); what triggers the transformation from planktonic to benthic life (Dreanno et al, 2006); and what genes are involved in such transformations (Hayward et al, 2011)? Despite the rapid increase in proteomics studies on nonmodel (where the genome has not been completely sequenced) species (Diz and Skibinski, 2007;McDonagh and Sheehan, 2006;Nunn and Timperman, 2007;Tomanek, 2006;Tomanek, 2011), proteins and their post-translational modifications (PTMs) involved in larval metamorphosis and calcification are still largely unknown (Chandramouli et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Proteomic response of marine invertebrate larvae to ocean acidification and hypoxia during metamorphosis and calcification

Mukherjee

Wong

Chandramouli

et al. 2013

Journal of Experimental Biology

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SUMMARYCalcifying marine invertebrates with complex life cycles are particularly at risk to climate changes as they undergo an abrupt ontogenetic shift during larval metamorphosis. Although our understanding of the larval response to climate changes is rapidly advancing, the proteome plasticity involved in a compensatory response to climate change is still unknown. In this study, we investigated the proteomic response of metamorphosing larvae of the tubeworm Hydroides elegans, challenged with two climate change stressors, ocean acidification (OA; pH 7.6) and hypoxia (HYP; 2.8 mg O 2 l −1 ), and with both combined. Using a twodimensional gel electrophoresis (2-DE)-based approach coupled with mass spectrometry, we found that climate change stressors did not affect metamorphosis except under OA, but altered the larval proteome and phosphorylation status. Metabolism and various stress and calcification-related proteins were downregulated in response to OA. In OA and HYP combined, HYP restored the expression of the calcification-related proteins to the control levels. We speculate that mild HYP stress could compensate for the negative effects of OA. This study also discusses the potential functions of selected proteins that might play important roles in larval acclimation and adaption to climate change.Supplementary material available online at http://jeb.biologists.org/lookup/suppl

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Recruitment in the sea: bacterial genes required for inducing larval settlement in a polychaete worm

Cited by 79 publications

References 43 publications

Development of a feeding trochophore in the polychaete Hydroides elegans

Development of a feeding trochophore in the polychaete Hydroides elegans

Animals in a bacterial world, a new imperative for the life sciences

Proteomic response of marine invertebrate larvae to ocean acidification and hypoxia during metamorphosis and calcification

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