Cryptic mtDNA Diversity of Diopatra cuprea (Onuphidae, Annelida) in the Northwestern Atlantic Ocean.

Marine annelid taxonomy is experiencing a period of rapid revision, with many previously "cosmopolitan" species being split into species with more limited geographic ranges. This is exemplified by the Diopatra genus, which has recently witnessed dozens of new species descriptions rooted in genetic analyses. In the northwestern Atlantic, the name D. cuprea (Bosc 1802) has been applied to populations from Cape Cod through the Gulf of Mexico, Central America, and Brazil. Here, we sequenced mitochondrial cytochrome oxidase I (COI) in D. cuprea populations from the Gulf of Mexico to Massachusetts. We find evidence for several deep mitochondrial lineages, suggesting that cryptic diversity is present in the D. cuprea complex from this coastline.

A Review of Diopatra Ecology: Current Knowledge, Open Questions, and Future Threats for an Ecosystem Engineering Polychaete.

A well-known example of marine ecosystem engineering is the annelid genus Diopatra, which builds large tubes in coastal sediments worldwide. Early studies of Diopatra were among the first to recognize the importance of facilitation in ecology, and Diopatra has become a key marine soft-sediment application of the ecosystem engineering concept. Here, I review our current knowledge of Diopatra ecology, including its natural history, ecosystem engineering effects, and trophic relationships. I particularly explore how human activities are influencing Diopatra in terms of climate change, bait fishing, and species invasions. Most of what we know about Diopatra ecology comes from focal studies of a few species in a few well-known regions. Further evaluating how our current understanding applies to other species and/or other regions will help to refine and deepen our understanding of structure and function in marine systems.

Origination and immigration drive latitudinal gradients in marine functional diversity.

Global patterns in the functional attributes of organisms are critical to understanding biodiversity trends and predicting biotic responses to environmental change. In the first global marine analysis, we find a strong decrease in functional richness, but a strong increase in functional evenness, with increasing latitude using intertidal-to-outer-shelf bivalves as a model system (N = 5571 species). These patterns appear to be driven by the interplay between variation in origination rates among functional groups, and latitudinal patterns in origination and range expansion, as documented by the rich fossil record of the group. The data suggest that (i) accumulation of taxa in spatial bins and functional categories has not impeded continued diversification in the tropics, and (ii) extinctions will influence ecosystem function differentially across latitudes.

Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient.

Latitudinal diversity gradients are underlain by complex combinations of origination, extinction, and shifts in geographic distribution and therefore are best analyzed by integrating paleontological and neontological data. The fossil record of marine bivalves shows, in three successive late Cenozoic time slices, that most clades (operationally here, genera) tend to originate in the tropics and then expand out of the tropics (OTT) to higher latitudes while retaining their tropical presence. This OTT pattern is robust both to assumptions on the preservation potential of taxa and to taxonomic revisions of extant and fossil species. Range expansion of clades may occur via "bridge species," which violate climate-niche conservatism to bridge the tropical-temperate boundary in most OTT genera. Substantial time lags (∼5 Myr) between the origins of tropical clades and their entry into the temperate zone suggest that OTT events are rare on a per-clade basis. Clades with higher diversification rates within the tropics are the most likely to expand OTT and the most likely to produce multiple bridge species, suggesting that high speciation rates promote the OTT dynamic. Although expansion of thermal tolerances is key to the OTT dynamic, most latitudinally widespread species instead achieve their broad ranges by tracking widespread, spatially-uniform temperatures within the tropics (yielding, via the nonlinear relation between temperature and latitude, a pattern opposite to Rapoport's rule). This decoupling of range size and temperature tolerance may also explain the differing roles of species and clade ranges in buffering species from background and mass extinctions.

Global environmental predictors of benthic marine biogeographic structure.

Analyses of how environmental factors influence the biogeographic structure of biotas are essential for understanding the processes underlying global diversity patterns and for predicting large-scale biotic responses to global change. Here we show that the large-scale geographic structure of shallow-marine benthic faunas, defined by existing biogeographic schemes, can be predicted with 89-100% accuracy by a few readily available oceanographic variables; temperature alone can predict 53-99% of the present-day structure along coastlines. The same set of variables is also strongly correlated with spatial changes in species compositions of bivalves, a major component of the benthic marine biota, at the 1° grid-cell resolution. These analyses demonstrate the central role of coastal oceanography in structuring benthic marine biogeography and suggest that a few environmental variables may be sufficient to model the response of marine biogeographic structure to past and future changes in climate.

Functional groups of ecosystem engineers: a proposed classification with comments on current issues.

Ecologists have long known that certain organisms fundamentally modify, create, or define habitats by altering the habitat's physical properties. In the past 15 years, these processes have been formally defined as "ecosystem engineering", reflecting a growing consensus that environmental structuring by organisms represents a fundamental class of ecological interactions occurring in most, if not all, ecosystems. Yet, the precise definition and scope of ecosystem engineering remains debated, as one should expect given the complexity, enormity, and variability of ecological systems. Here I briefly comment on a few specific current points of contention in the ecosystem engineering concept. I then suggest that ecosystem engineering can be profitably subdivided into four narrower functional categories reflecting four broad mechanisms by which ecosystem engineering occurs: structural engineers, bioturbators, chemical engineers, and light engineers. Finally, I suggest some conceptual model frameworks that could apply broadly within these functional groups.

Sublethal predation and regeneration in two onuphid polychaetes: patterns and implications.

We examined sublethal predation in the polychaete Diopatra cuprea, an important ecosystem engineer of intertidal and shallow subtidal marine sediments in the western Atlantic. D. cuprea commonly loses its antennae and portions of its anterior to predator attacks; these lost body portions are subsequently regenerated. We asked (i) if the intensity of sublethal predation differs for D. cuprea populations in Virginia versus Florida, (ii) if sublethal predation varies temporally in each region, and (iii) if sublethal predation influences activity and tube-building rates. Within Florida, we also drew comparisons between D. cuprea and the closely related onuphid Americonuphis magna. Surprisingly, we found that sublethal predation is more intense in Virginia than in Florida, likely making substantial contributions to secondary productivity. Within Florida, A. magna experienced more antennal loss than D. cuprea and is incapable of anterior regeneration. D. cuprea activity and tube-building rates are strongly influenced by anterior loss, but more subtly influenced by antennal loss. Given the observed rates of sublethal predation and population densities in Virginia versus Florida, sublethal predation is an important factor influencing D. cuprea populations and their associated communities.

Tube decoration may not be cryptic for Diopatra cuprea (Polychaeta: Onuphidae).

Previous studies have suggested several adaptive functions for the decorated tube caps of Diopatra cuprea (Polychaeta: Onuphidae). We experimentally tested the hypothesis that decoration provides crypsis. A series of field experiments quantified predation-related damage done to tube caps that were (1) devoid of decoration, (2) decorated with algae, or (3) decorated with shell fragments. If decoration provides crypsis, then undecorated tube caps should experience more damage than decorated tube caps; this pattern was not observed. Decoration may still reduce predation rates by means other than crypsis, but these results strongly suggest that tube decoration does not interfere with predator recognition of D. cuprea tube caps and that crypsis is consequently not important in this system.

Defining the role of ubiquitin-interacting motifs in the polyglutamine disease protein, ataxin-3.

Polyglutamine (polyQ) expansions cause neurodegeneration that is associated with protein misfolding and influenced by functional properties of the host protein. The polyQ disease protein, ataxin-3, has predicted ubiquitin-specific protease and ubiquitin-binding domains, which suggest that ataxin-3 functions in ubiquitin-dependent protein surveillance. Here we investigate direct links between the ubiquitin-proteasome pathway and ataxin-3. In neural cells we show that, through its ubiquitin interaction motifs (UIMs), normal or expanded ataxin-3 binds a broad range of ubiquitinated proteins that accumulate when the proteasome is inhibited. The expression of a catalytically inactive ataxin-3 (normal or expanded) causes ubiquitinated proteins to accumulate in cells, even in the absence of proteasome inhibitor. This accumulation of ubiquitinated proteins occurs primarily in the cell nucleus in transfected cells and requires intact UIMs in ataxin-3. We further show that both normal and expanded ataxin-3 can undergo oligoubiquitination. Although this post-translational modification occurs in a UIM-dependent manner, it becomes independent of UIMs when the catalytic cysteine residue of ataxin-3 is mutated, suggesting that ataxin-3 ubiquitination is itself regulated in trans by its own de-ubiquitinating activity. Finally, pulse-chase labeling reveals that ataxin-3 is degraded by the proteasome, with expanded ataxin-3 being as efficiently degraded as normal ataxin-3. Mutating the UIMs does not alter degradation, suggesting that UIM-mediated oligoubiquitination of ataxin-3 modulates ataxin-3 function rather than stability. The function of ataxin-3 as a de-ubiquitinating enzyme, its post-translational modification by ubiquitin, and its degradation via the proteasome link this polyQ protein to ubiquitin-dependent pathways already implicated in disease pathogenesis.

Caspase-mediated proteolysis of the polyglutamine disease protein ataxin-3.

Spinocerebellar ataxia type-3, also known as Machado-Joseph Disease, is one of many inherited neurodegenerative disorders caused by polyglutamine-encoding CAG repeat expansions in otherwise unrelated disease genes. Polyglutamine disorders are characterized by disease protein misfolding and aggregation; often within the nuclei of affected neurons. Although the precise mechanism of polyglutamine-mediated cell death remains elusive, evidence suggests that proteolysis of polyglutamine disease proteins by caspases contributes to pathogenesis. Using cellular models we now show that the endogenous spinocerebellar ataxia type-3 disease protein, ataxin-3, is proteolyzed in apoptotic paradigms, resulting in the loss of full-length ataxin-3 and the corresponding appearance of an approximately 28-kDa fragment containing the glutamine repeat. Broad-spectrum caspase inhibitors block ataxin-3 proteolysis and studies suggest that caspase-1 is a primary mediator of cleavage. Site-directed mutagenesis experiments eliminating three, six or nine potential caspase cleavage sites in the protein suggest redundancy in the site(s) at which cleavage can occur, as previously described for other disease proteins; but also map a major cleavage event to a cluster of aspartate residues within the ubiquitin-binding domain of ataxin-3 near the polyglutamine tract. Finally, caspase-mediated cleavage of expanded ataxin-3 resulted in increased ataxin-3 aggregation, suggesting a potential role for caspase-mediated proteolysis in spinocerebellar ataxia type-3 pathogenesis.

Poly-ubiquitin binding by the polyglutamine disease protein ataxin-3 links its normal function to protein surveillance pathways.

In at least nine inherited diseases polyglutamine expansions cause neurodegeneration associated with protein misfolding and the formation of ubiquitin-conjugated aggregates. Although expanded polyglutamine triggers disease, functional properties of host polyglutamine proteins also must influence pathogenesis. Using complementary in vitro and cell-based approaches we establish that the polyglutamine disease protein, ataxin-3, is a poly-ubiquitin-binding protein. In stably transfected neural cell lines, normal and expanded ataxin-3 both co-precipitate with poly-ubiquitinated proteins that accumulate when the proteasome is inhibited. In vitro pull-down assays show that this reflects direct interactions between ataxin-3 and higher order ubiquitin conjugates; ataxin-3 binds K48-linked tetraubiquitin but not di-ubiquitin or mono-ubiquitin. Further studies with domain-deleted and site-directed mutants map tetra-ubiquitin binding to ubiquitin interaction motifs situated near the polyglutamine domain. In surface plasmon resonance binding analyses, normal and expanded ataxin-3 display similar submicromolar dissociation constants for tetra-ubiquitin. Binding kinetics, however, are markedly influenced by the surrounding protein context; ataxin-3 that lacks the highly conserved, amino-terminal josephin domain shows significantly faster association and dissociation rates for tetra-ubiquitin binding. Our results establish ataxin-3 as a poly-ubiquitin-binding protein, thereby linking its normal function to protein surveillance pathways already implicated in polyglutamine pathogenesis.

Protein aggregation and the ubiquitin proteasome pathway: gaining the UPPer hand on neurodegeneration.

Protein misfolding and aggregation are common to most neurodegenerative diseases, suggesting that abnormalities of protein homeostasis contribute to pathogenesis. Research implicates at least two components of cellular protein quality control in disease: molecular chaperones and the ubiquitin-proteasome pathway (UPP). Although evidence is more compelling for chaperone involvement, recent cell-based and genetic studies suggest that perturbations in the UPP also contribute to neurodegenerative disease processes. UPP involvement in disease seems even more probable when the UPP is viewed not simply as an isolated degradation machine but rather as a complex cascade linked both to other ubiquitin-dependent processes and to chaperone systems.