scholarly journals Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails

2020 ◽  
Vol 37 (12) ◽  
pp. 3469-3484
Author(s):  
Corinna Breusing ◽  
Shannon B Johnson ◽  
Verena Tunnicliffe ◽  
David A Clague ◽  
Robert C Vrijenhoek ◽  
...  

Abstract Despite significant advances in our understanding of speciation in the marine environment, the mechanisms underlying evolutionary diversification in deep-sea habitats remain poorly investigated. Here, we used multigene molecular clocks and population genetic inferences to examine processes that led to the emergence of the six extant lineages of Alviniconcha snails, a key taxon inhabiting deep-sea hydrothermal vents in the Indo-Pacific Ocean. We show that both allopatric divergence through historical vicariance and ecological isolation due to niche segregation contributed to speciation in this genus. The split between the two major Alviniconcha clades (separating A. boucheti and A. marisindica from A. kojimai, A. hessleri, and A. strummeri) probably resulted from tectonic processes leading to geographic separation, whereas the splits between co-occurring species might have been influenced by ecological factors, such as the availability of specific chemosynthetic symbionts. Phylogenetic origin of the sixth species, Alviniconcha adamantis, remains uncertain, although its sister position to other extant Alviniconcha lineages indicates a possible ancestral relationship. This study lays a foundation for future genomic studies aimed at deciphering the roles of local adaptation, reproductive biology, and host–symbiont compatibility in speciation of these vent-restricted snails.

2020 ◽  
Author(s):  
Yi Lan ◽  
Jin Sun ◽  
Chong Chen ◽  
Yanan Sun ◽  
Yadong Zhou ◽  
...  

AbstractAnimals endemic to deep-sea hydrothermal vents often form obligatory relationships with bacterial symbionts, maintained by intricate host-symbiont interactions. Endosymbiosis with more than one symbiont is uncommon, and most genomic studies focusing on such ‘dual symbiosis’ systems have not investigated the host and the symbionts to a similar depth simultaneously. Here, we report a novel dual symbiosis among the peltospirid snail Gigantopelta aegis and its two Gammaproteobacteria endosymbionts – one being a sulphur oxidiser and the other a methane oxidiser. We assembled high-quality genomes for all three parties of this holobiont, with a chromosome-level assembly for the snail host (1.15 Gb, N50 = 82 Mb, 15 pseudo-chromosomes). In-depth analyses of these genomes reveal an intimate mutualistic relationship with complementarity in nutrition and metabolic codependency, resulting in a system highly versatile in transportation and utilisation of chemical energy. Moreover, G. aegis has an enhanced immune capability that likely facilitates the possession of more than one type of symbiont. Comparisons with Chrysomallon squamiferum, another chemosymbiotic snail in the same family but only with one sulphur-oxidising endosymbiont, show that the two snails’ sulphur-oxidising endosymbionts are phylogenetically distant, agreeing with previous results that the two snails have evolved endosymbiosis independently and convergently. Notably, the same capabilities of biosynthesis of specific nutrition lacking in the host genome are shared by the two sulphur-oxidising endosymbionts of the two snail genera, which may be a key criterion in the selection of symbionts by the hosts.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Yi Lan ◽  
Jin Sun ◽  
Chong Chen ◽  
Yanan Sun ◽  
Yadong Zhou ◽  
...  

AbstractAnimals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host–symbiont interactions. Most genomic studies on holobionts have not investigated both sides to similar depths. Here, we report dual symbiosis in the peltospirid snail Gigantopelta aegis with two gammaproteobacterial endosymbionts: a sulfur oxidiser and a methane oxidiser. We assemble high-quality genomes for all three parties, including a chromosome-level host genome. Hologenomic analyses reveal mutualism with nutritional complementarity and metabolic co-dependency, highly versatile in transporting and using chemical energy. Gigantopelta aegis likely remodels its immune system to facilitate dual symbiosis. Comparisons with Chrysomallon squamiferum, a confamilial snail with a single sulfur-oxidising gammaproteobacterial endosymbiont, show that their sulfur-oxidising endosymbionts are phylogenetically distant. This is consistent with previous findings that they evolved endosymbiosis convergently. Notably, the two sulfur-oxidisers share the same capabilities in biosynthesising nutrients lacking in the host genomes, potentially a key criterion in symbiont selection.


2001 ◽  
Vol 67 (10) ◽  
pp. 4566-4572 ◽  
Author(s):  
Barbara J. Campbell ◽  
Christian Jeanthon ◽  
Joel E. Kostka ◽  
George W. Luther ◽  
S. Craig Cary

ABSTRACT Recent molecular characterizations of microbial communities from deep-sea hydrothermal sites indicate the predominance of bacteria belonging to the epsilon subdivision of Proteobacteria(epsilon Proteobacteria). Here, we report the first enrichments and characterizations of four epsilonProteobacteria that are directly associated withAlvinella pompejana, a deep sea hydrothermal vent polychete, or with hydrothermal vent chimney samples. These novel bacteria were moderately thermophilic sulfur-reducing heterotrophs growing on formate as the energy and carbon source. In addition, two of them (Am-H and Ex-18.2) could grow on sulfur lithoautrotrophically using hydrogen as the electron donor. Optimal growth temperatures of the bacteria ranged from 41 to 45°C. Phylogenetic analysis of the small-subunit ribosomal gene of the two heterotrophic bacteria demonstrated 95% similarity to Sulfurospirillum arcachonense, an epsilon Proteobacteria isolated from an oxidized marine surface sediment. The autotrophic bacteria grouped within a deeply branching clade of the epsilonProteobacteria, to date composed only of uncultured bacteria detected in a sample from a hydrothermal vent along the mid-Atlantic ridge. A molecular survey of various hydrothermal vent environments demonstrated the presence of two of these bacteria (Am-N and Am-H) in more than one geographic location and habitat. These results suggest that certain epsilonProteobacteria likely fill important niches in the environmental habitats of deep-sea hydrothermal vents, where they contribute to overall carbon and sulfur cycling at moderate thermophilic temperatures.


Author(s):  
Sabine Stöhr ◽  
Michel Segonzac

The animal communities associated with the deep-sea reducing environment have been studied for almost 30 years, but until now only a single species of ophiuroid, Ophioctenella acies, has been found at both hydrothermal vents and methane cold seeps. Since the faunal overlap between vent and seep communities is small and many endemic species have been found among other taxa (e.g. Mollusca, Crustacea), additional species of ophiuroids were expected at previously unstudied sites. Chemical compositions at reducing sites differ greatly from the nearby bathyal environment. Generally, species adapted to chemosynthetic environments are not found in non-chemosynthetic habitats, but occasional visitors of other bathyal species to vent and seep sites have been recorded among many taxa except ophiuroids. This paper presents an analysis of the ophiuroid fauna found at hydrothermal vents and non-reducing nearby sites on the Mid-Atlantic Ridge and on methane cold seeps in the Gulf of Mexico, at Blake Ridge off South Carolina and south of Barbados. In addition to O. acies, four species were found at vents, Ophiactis tyleri sp. nov., Ophiocten centobi, Ophiomitra spinea and Ophiotreta valenciennesi rufescens. While Ophioctenella acies appears to be restricted to chemosynthetic areas, the other four species were also found in other bathyal habitats. They also occur in low numbers (mostly single individuals), whereas species adapted to hydrothermal areas typically occur in large numbers. Ophioscolex tripapillatus sp. nov. and Ophiophyllum atlanticum sp. nov. are described from nearby non-chemosynthetic sites. In a cold seep south of Barbados, three species of ophiuroids were found, including Ophioctenella acies, Amphiura sp., Ophiacantha longispina sp. nov. and Ophioplinthaca chelys. From the cold seeps at Blake Ridge and the Gulf of Mexico, Ophienigma spinilimbatum gen. et sp. nov. is described, likely restricted to the reducing environment. Ophiotreta valenciennesi rufescens occurred abundantly among Lophelia corals in the Gulf of Mexico seeps, which is the first record of this species from the West Atlantic. Habitat descriptions complement the taxonomic considerations, and the distribution of the animals in reducing environments is discussed.


1991 ◽  
Vol 159 (1) ◽  
pp. 473-487 ◽  
Author(s):  
ELIZABETH DAHLHOFF ◽  
GEORGE N. SOMERO

Effects of temperature and hydrostatic pressure were measured on cytosolic malate dehydrogenases (cMDHs) from muscle tissue of a variety of shallow- and deep-living benthic marine invertebrates, including seven species endemic to the deep-sea hydrothermal vents. The apparent Michaelis-Menten constant (Km) of coenzyme (nicotinamide adenine dinucleotide, NADH), used to index temperature and pressure effects, was conserved within a narrow range (approximately 15–25 μmoll−1) at physiological temperatures and pressures for all species. However, at elevated pressures, the Km of NADH rose sharply for cMDHs of shallow species (depths of occurrence >Approximately 500 m), but not for the cMDHs of deep-sea species. Cytosolic MDHs of invertebrates from the deep-sea hydrothermal vents generally were not perturbed by elevated temperatures (15–25°C) at in situ pressures, but cMDHs of cold-adapted deep-sea species were. At a single measurement temperature, the Km of NADH for cMDHs from invertebrates from habitats with well-characterized temperatures was inversely related to maximal sustained body temperature. This correlation was used to predict the maximal sustained body temperatures of vent invertebrates for which maximal habitat and body temperatures are difficult to estimate. Species occurring on the ‘smoker chimneys’, which emit waters with temperatures up to 380°C, are predicted to have sustained body temperatures that are approximately 20–25°C higher than vent species living in cooler vent microhabitats. We conclude that, just as adaptation of enzymes to elevated pressures is important in establishing species’ depth distribution patterns, adaptation of pressure-adapted enzymes to temperature is critical in enabling certain vent species to exploit warm-water microhabitats in the vent environment.


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