Mesenchytraeus Solifugus Research Articles

The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress.

The inorganic polymer, polyphosphate (polyP), is present in all organisms examined to date with putative functions ranging from the maintenance of bioenergetics to stress resilience and protein homeostasis. Bioenergetics in the glacier-obligate, segmented worm, Mesenchytraeus solifugus, is characterized by a paradoxical increase in intracellular ATP levels as temperatures decline. We show here that steady-state, mitochondrial polyP levels vary among species of Annelida, but were elevated only in M. solifugus in response to thermal stress. In contrast, polyP levels decreased with temperature in the mesophilic worm, Enchytraeus crypticus. These results identify fundamentally different bioenergetic strategies between closely related annelid worms, and suggest that I worm mitochondria maintain ATP and polyP in a dynamic equilibrium.

Structural Evolution of the Glacier Ice Worm Fo ATP Synthase Complex.

The segmented annelid worm, Mesenchytraeus solifugus, is a permanent resident of temperate, maritime glaciers in the Pacific northwestern region of North America, displaying atypically high intracellular ATP levels which have been linked to its unusual ability to thrive in hydrated glacier ice. We have shown previously that ice worms contain a highly basic, carboxy terminal extension on their ATP6 regulatory subunit, likely acquired by horizontal gene transfer from a microbial dietary source. Here we examine the full complement of F1F0 ATP synthase structural subunits with attention to non-conservative, ice worm-specific structural modifications. Our genomics analyses and molecular models identify putative proton shuttling domains on either side of the F0 hemichannel, which predictably function to enhance proton flow across the mitochondrial membrane. Other components of the ice worm ATP synthase complex have remained largely unchanged in the context of Metazoan evolution.

Long-distance dispersal, ice sheet dynamics and mountaintop isolation underlie the genetic structure of glacier ice worms.

Disentangling the contemporary and historical factors underlying the spatial distributions of species is a central goal of biogeography. For species with broad distributions but little capacity to actively disperse, disconnected geographical distributions highlight the potential influence of passive, long-distance dispersal (LDD) on their evolutionary histories. However, dispersal alone cannot completely account for the biogeography of any species, and other factors-e.g. habitat suitability, life history-must also be considered. North American ice worms ( Mesenchytraeus solifugus) are ice-obligate annelids that inhabit coastal glaciers from Oregon to Alaska. Previous studies identified a complex biogeographic history for ice worms, with evidence for genetic isolation, unexpectedly close relationships among geographically disjunct lineages, and contemporary migration across large (e.g. greater than 1500 km) areas of unsuitable habitat. In this study, we analysed genome-scale sequence data for individuals from most of the known ice worm range. We found clear support for divergence between populations along the Pacific Coast and the inland flanks of the Coast Mountains (mean FST = 0.60), likely precipitated by episodic ice sheet expansion and contraction during the Pleistocene. We also found support for LDD of ice worms from Alaska to Vancouver Island, perhaps mediated by migrating birds. Our results highlight the power of genomic data for disentangling complex biogeographic patterns, including the presence of LDD.

Atypical Evolution of the F1Fo Adenosine Triphosphate Synthase Regulatory ATP6 subunit in Glacier Ice Worms (Annelida: Clitellata: Mesenchytraeus).

The glacier ice worm, Mesenchytraeus solifugus, is among a few animals that reside permanently in glacier ice. Their adaptation to cold temperature has been linked to relatively high intracellular adenosine triphosphate (ATP) levels, which compensate for reductions in molecular motion at low physiological temperatures. Here, we show that ATP6—the critical regulatory subunit of the F1Fo-ATP synthase and primary target of mitochondrial disease—acquired an unprecedented histidine-rich, 18-amino acid carboxy-terminal extension, which counters the strong evolutionary trend of mitochondrial genome compaction. Furthermore, sequence analysis suggests that this insertion is not of metazoan origin, but rather is a product of horizontal gene transfer from a microbial dietary source, and may act as a proton shuttle to accelerate the rate of ATP synthesis.

Bacterial Microbiota Associated with the Glacier Ice Worm Is Dominated by Both Worm-Specific and Glacier-Derived Facultative Lineages.

The community structure of bacteria associated with the glacier ice worm Mesenchytraeus solifugus was analyzed by amplicon sequencing of 16S rRNA genes and their transcripts. Ice worms were collected from two distinct glaciers in Alaska, Harding Icefield and Byron Glacier, and glacier surfaces were also sampled for comparison. Marked differences were observed in bacterial community structures between the ice worm and glacier surface samples. Several bacterial phylotypes were detected almost exclusively in the ice worms, and these bacteria were phylogenetically affiliated with either animal-associated lineages or, interestingly, clades mostly consisting of glacier-indigenous species. The former included bacteria that belong to Mollicutes, Chlamydiae, Rickettsiales, and Lachnospiraceae, while the latter included Arcicella and Herminiimonas phylotypes. Among these bacteria enriched in ice worm samples, Mollicutes, Arcicella, and Herminiimonas phylotypes were abundantly and consistently detected in the ice worm samples; these phylotypes constituted the core microbiota associated with the ice worm. A fluorescence in situ hybridization analysis showed that Arcicella cells specifically colonized the epidermis of the ice worms. Other bacterial phylotypes detected in the ice worm samples were also abundantly recovered from the respective habitat glaciers; these bacteria may be food for ice worms to digest or temporary residents. Nevertheless, some were overrepresented in the ice worm RNA samples; they may also function as facultative gut bacteria. Our results indicate that the community structure of bacteria associated with ice worms is distinct from that in the associated glacier and includes worm-specific and facultative, glacier-indigenous lineages.

The Role of Temperature in the Distribution of the Glacier Ice Worm, Mesenchytraeus solifugus (Annelida: Oligochaeta: Enchytraeidae)

ABSTRACTThe North American glacier ice worm, Mesenchytraeus solifugus (Emery, 1898), is restricted to coastal glaciers in the American Pacific Northwest with a puzzling 400 km distribution gap along the Alaska–British Columbia border and several disjunct populations of northern clades in southern latitudes. We illustrate the role of minimum temperatures in ice worm behavior, abundance, and distribution. The study included 200 glaciers and 25 mitochondrial CO1 haplotypes from the species' 5 × 105 km2 geographic range. Minimum winter temperatures on the previous summer surface appear to determine: (1) the elevations ice worms occupy, (2) the glaciers that can support them, and (3) the mountain ranges they inhabit. Ice worms do not inhabit glaciers with over-winter temperatures below −7 °C on the previous summer surface. An annelid molecular clock in a Bayesian phylogeny suggests ice worms diverged from an aquatic ancestor 2.23 Ma, emerging as three clades 1.6–1.7 Ma. Cold sensitivity, together with southeast Alaska’s geography and past climate, likely created the distribution gap, a hypothesis supported by their phylogeography.

Census of bacterial microbiota associated with the glacier ice worm Mesenchytraeus solifugus.

The glacier ice worm, Mesenchytraeus solifugus, is a unique annelid, inhabiting only snow and ice in North American glaciers. Here, we analyzed the taxonomic composition of bacteria associated with M. solifugus based on the 16S rRNA gene. We analyzed four fixed-on-site and 10 starved ice worm individuals, along with glacier surface samples. In total, 1341 clones of 16S rRNA genes were analyzed for the ice worm samples, from which 65 bacterial phylotypes (99.0% cut-off) were identified. Of these, 35 phylotypes were closely related to sequences obtained from their habitat glacier and/or other components of cryosphere; whereas three dominant phylotypes were affiliated with animal-associated lineages of the class Mollicutes. Among the three, phylotype Ms-13 shared less than 89% similarity with database sequences and was closest to a gut symbiont of a terrestrial earthworm. Using fluorescence in situ hybridization, Ms-13 was located on the gut wall surface of the ice worms. We propose a novel genus and species, 'Candidatus Vermiplasma glacialis', for this bacterium. Our results raise the possibility that the ice worm has exploited indigenous glacier bacteria, while several symbiotic bacterial lineages have maintained their association with the ice worm during the course of adaptive evolution to the permanently cold environment.

Cold-adapted tubulins in the glacier ice worm, Mesenchytraeus solifugus

Glacier ice worms, Mesenchytraeus solifugus and related species, are the only known annelids that survive obligately in glacier ice and snow. One fundamental component of cold temperature adaptation is the ability to polymerize tubulin, which typically depolymerizes at low physiological temperatures (e.g., < 10 °C) in most temperate species. In this study, we isolated two α-tubulin (Msα1, Msα2) and two β-tubulin (Msβ1, Msβ2) subunits from an ice worm cDNA library, and compared their predicted amino acid sequences with homologues from other cold-adapted organisms (e.g., Antarctic fish, ciliate) in an effort to identify species-specific amino acid substitutions that contribute to cold temperature-dependent tubulin polymerization. Our comparisons and predicted protein structures suggest that ice worm-specific amino acid substitutions stabilize lateral contact associations, particularly between β-tubulin protofilaments, but these substitutions occur at different positions in comparison with other cold-adapted tubulins. The ice worm tubulin gene family appears relatively small, comprising one primary α- and one primary β-tubulin monomers, though minor isoforms and psuedogenes were identified. Our analyses suggest that variation occurs in the strategies (i.e., species-specific amino acid substitutions, gene number) by which cold-adapted taxa have evolved the ability to polymerize tubulin at low physiological temperatures.

Distribution and phylogeny of glacier ice worms (Mesenchytraeus solifugus and Mesenchytraeus solifugus rainierensis)

Glacier ice worms, Mesenchytraeus solifugus (Emery, 1898) and Mesenchytraeus solifugus rainierensis Welch, 1916 (Enchytraeidae), are the only known oligochaetes adapted to life in ice. We have collected ice worm specimens from over 100 populations throughout the Pacific northwestern region of North America. Their current range extends ~2500 km along the Pacific coastline between south-central Alaska and central Oregon, with most populations occurring on relatively low-elevation, temperate glaciers. Phylogenetic analyses utilizing partial nuclear 28S rDNA and mitochondrial cytochrome c oxidase subunit I (COI) loci revealed the presence of two geographically distinct clades (northern and southern). The northern clade comprises all Alaskan populations, while the southern clade contains British Columbia, Washington State, and Oregon State populations. No evidence of gene flow was detected between these two lineages or between noncontiguous glaciers throughout their geographic range. Our results suggest that the mechanism of ice worm dispersal is primarily active, though at least one episode of passive dispersal is noted at the southern extent of their range.

Molecular Adaptation in the Ice Worm, Mesenchytraeus solifugus: Divergence of Energetic-Associated Genes

The ice worm, Mesenchytraeus solifugus, is the largest glacially obligate metazoan and among only a few metazoan species that complete their life cycle at 0 degrees C. We conducted a large-scale sequencing analysis of cDNAs isolated from ice worm anterior segments. Sequence comparisons among an available group of ice worm, arthropod, chordate, and nematode homologues suggest that ice worms encode proteins that are less bulky, are less polar, and contain fewer charged residues. Also, subunits of the catalytic F1 ATP synthase complex appear to have diverged more rapidly than other ice worm genes examined, suggesting a role in cold-temperature adaptation. Modeling of F1 ATP synthase beta and gamma subunits identified nonconservative, ice worm-specific amino acid substitutions at subunit contact sites and at sites proximal to the catalytic site.

The ice worm, Mesenchytraeus solifugus, elevates adenylate levels at low physiological temperature

The ice worm, Mesenchytraeus solifugus, is among a few metazoan species that survive exclusively in glacier ice/snow. In this study, we demonstrate that ice worm adenylate levels [i.e. adenosine 5′-triphosphate (ATP), ADP and AMP] are maintained at levels well above their mesophilic counterparts, and that their response to temperature change is distinctly opposite, namely, ice worms increase energy levels as temperatures fall. Initially, this response is characterized by a sharp spike in [ATP] and the adenylate energy charge (even at sub-zero temperatures), which is followed by corresponding increases in [ADP] and [AMP] within a few days. These results suggest that ice worms have evolved a compensatory mechanism by which gains in adenylate nucleotides off-set, at least in part, the inherent lethargy and death usually associated with cold temperature.

Distribution and behavior of ice worms (Mesenchytraeus solifugus) in south-central Alaska

The ice worm, Mesenchytraeus solifugus ssp. rainierensis, is the only known annelid that survives in glacier ice. We report the locations of eight ice worm populations in south-central Alaska, including the northern- and western-most extent of known ice worm habitation. All ice worms identified in this study inhabit coastal glaciers proximal to the Gulf of Alaska. They were found in a variety of habitats including level snowfields, steep avalanche cones, crevasse walls, glacial rivers and pools, and hard glacier ice. Ice worms were not found on all coastal glaciers nor were they found in Alaska's interior (the Alaska Range). Ice worms on Byron Glacier, Alaska, totaled ~30 million and were distributed on seven distinct avalanche cones. They displayed a diurnal cycle, appearing on the glacier surface several hours before sunset and penetrating back into the glacier shortly after sunrise. Experiments suggest that ice worms preferentially penetrate the glacier beneath surface algae, Chlamydomonas nivalis, to a depth between 15 and 100 cm and resurface at a proximal location. Lateral movement of ice worms on the glacier surface can reach speeds of ~3 m/h. Ice worms on Byron Glacier avoided light, but did not respond preferentially to different wavelengths in the visible spectrum. Finally, ice worms displayed an unexpected attraction to heat.

Distribution and behavior of ice worms (&lt;i&gt;Mesenchytraeus solifugus&lt;/i&gt;) in south-central Alaska

The ice worm, Mesenchytraeus solifugus ssp. rainierensis, is the only known annelid that survives in glacier ice. We report the locations of eight ice worm populations in south-central Alaska, including the northern- and western-most extent of known ice worm habitation. All ice worms identified in this study inhabit coastal glaciers proximal to the Gulf of Alaska. They were found in a variety of habitats including level snowfields, steep avalanche cones, crevasse walls, glacial rivers and pools, and hard glacier ice. Ice worms were not found on all coastal glaciers nor were they found in Alaska's interior (the Alaska Range). Ice worms on Byron Glacier, Alaska, totaled ~30 million and were distributed on seven distinct avalanche cones. They displayed a diurnal cycle, appearing on the glacier surface several hours before sunset and penetrating back into the glacier shortly after sunrise. Experiments suggest that ice worms preferentially penetrate the glacier beneath surface algae, Chlamydomonas nivalis, to ...

Morphologic characterization of the ice worm Mesenchytraeus solifugus.

Ice worms occupy a unique position in metazoan phylogeny in that they are the only known annelid that completes its life cycle in ice. The mechanism(s) associated with this adaptation are likely to occur at different levels, ranging from modification of their metabolism to changes in morphology. In this study, we examined specimens of Mesenchytraeus solifugus by scanning electron microscopy (SEM) and transmission electron microscopy (TEM) in an effort to identify morphologic structures that may aid in its glacial habitation. We report that M. solifugus contains an elongated head pore at the tip of its prostomium, numerous sensory structures, and differentially oriented setae that curve abruptly at their distal end.

The geographical distribution of ice worms (O1igochaeta:Enchytraeidae)

Ice worms (Mesenchytraeus solifugus (Emery 1898)) have been found on the western coastal glaciers of North America, from the Bagley Icefield in Alaska, to Mt. Rainier, in Washington State. They are absent from the western interior and from the Central Alaska Ranges. It is speculated that their southern limit is north of the Columbia River, since this area represents the probable southern limit of Cordilleran ice.