Mussel larvae modify calcifying fluid carbonate chemistry to promote calcification

Ramesh, Kirti; Hu, Marian Yong-An; Thomsen, Jörn; Bleich, Markus; Melzner, Frank

doi:10.1038/s41467-017-01806-8

Cited by 78 publications

(77 citation statements)

References 43 publications

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“…In addition to the active transport of H + , secondary H + transport pathways such as voltage‐gated hydrogen channels also exhibited dynamic expression profiles during development of M. edulis . Proton efflux via voltage‐gated hydrogen channels are responsible for pH homeostasis in calcifying coccolithophore cells, preventing cytoplasmic acidification (Taylor, Chrachri, Wheeler, Goddard, & Brownlee, ).The elevated expression of H + transport pathways during larval calcification is consistent with the requirement to extrude protons that are generated by the mineralization of calcium carbonate from HCO 3 − and the observed increases in pH at the site of calcification in larval mussels (Ramesh et al, ).…”

Section: Discussionsupporting

confidence: 71%

“…Further, seawater C T reductions were associated with a decrease in p CO 2 from 423.4 ± 7.2 µatm under control conditions to 244.6 ± 23.7 µatm and Ω aragonite from 1.7 ± 0.03 to 0.6 ± 0.08. Development at reduced C T resulted in a developmental delay starting at 22 hpf, corresponding to the onset of calcification (Ramesh et al, , Figure , Table ). The mean developmental delay was 1.71 ± 1.38 hr, and in one family, the delay was observed to go up to 6 hr (Table ).…”

Section: Resultsmentioning

confidence: 99%

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Expression of calcification‐related ion transporters during blue mussel larval development

Ramesh

Yarra

Clark

et al. 2019

Ecology and Evolution

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The physiological processes driving the rapid rates of calcification in larval bivalves are poorly understood. Here, we use a calcification substrate‐limited approach (low dissolved inorganic carbon, CT) and mRNA sequencing to identify proteins involved in bicarbonate acquisition during shell formation. As a secondary approach, we examined expression of ion transport and shell matrix proteins (SMPs) over the course of larval development and shell formation. We reared four families of Mytilus edulis under ambient (ca. 1865 µmol/kg) and low CT (ca. 941 µmol/kg) conditions and compared expression patterns at six developmental time points. Larvae reared under low CT exhibited a developmental delay, and a small subset of contigs was differentially regulated between ambient and low CT conditions. Of particular note was the identification of one contig encoding an anion transporter (SLC26) which was strongly upregulated (2.3–2.9 fold) under low CT conditions. By analyzing gene expression profiles over the course of larval development, we are able to isolate sequences encoding ion transport and SMPs to enhance our understanding of cellular pathways underlying larval calcification processes. In particular, we observe the differential expression of contigs encoding SLC4 family members (sodium bicarbonate cotransporters, anion exchangers), calcium‐transporting ATPases, sodium/calcium exchangers, and SMPs such as nacrein, tyrosinase, and transcripts related to chitin production. With a range of candidate genes, this work identifies ion transport pathways in bivalve larvae and by applying comparative genomics to investigate temporal expression patterns, provides a foundation for further studies to functionally characterize the proteins involved in larval calcification.

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Section: Discussionsupporting

confidence: 71%

Section: Resultsmentioning

confidence: 99%

Expression of calcification‐related ion transporters during blue mussel larval development

Ramesh

Yarra

Clark

et al. 2019

Ecology and Evolution

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“…During mid-veliger stages, from 6 to 16 dpf, we observed no discernable differences in survival or growth rate of veliger larvae in either water treatment, broodstock group or experiment. Shelled veliger larvae are somewhat more resilient to elevated seawater pCO 2 and low Ω arag (Ramesh et al 2017), but these conditions have nevertheless been shown to exhibit distinct effects on the physiology of larval oysters. Timmins-Schiffman et al (2013) and Frieder et al (2017) indicated that acidified seawater reduces net calcification rates of early larvae, and Pan et al (2015) and Frieder et al (2018) suggested that acidification stress alters the allocation of metabolic energy within larvae.…”

Section: Veliger Growth and Survivalmentioning

confidence: 99%

Comparison of larval development in domesticated and naturalized stocks of the Pacific oyster Crassostrea gigas exposed to high pCO2 conditions

Durland¹,

Waldbusser²,

Langdon³

2019

Mar. Ecol. Prog. Ser.

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Ocean acidification (OA) has had significant negative effects on oyster populations on the west coast of North America over the past decade. Many studies have focused on the physiological challenges experienced by young oyster larvae in high pCO 2 /low pH seawater with reduced aragonite saturation state (Ω arag), which is characteristic of OA. Relatively few, by contrast, have evaluated these impacts upon fitness traits across multiple larval stages and between discrete oyster populations. In this study, we conducted 2 replicated experiments, in 2015 and 2016, using larvae from naturalized 'wild' and selectively bred stocks of the Pacific oyster Crassostrea gigas from the US Pacific Northwest and reared them in ambient (~400 µatm) or high (~1600 µatm) pCO 2 seawater from fertilization through final metamorphosis to juvenile 'spat.' In each year, high pCO 2 seawater inhibited early larval development and affected the timing, but not the magnitude, of mortality during this stage. The effects of acidified seawater on metamorphosis of pediveligers to spat were variable between years, with no effect of seawater pCO 2 in the first experiment but a ~42% reduction in spat in the second. Despite this variability, larvae from selectively bred oysters produced, on average, more (+ 55 and 37%) and larger (+ 5 and 23%) spat in ambient and high pCO 2 seawater, respectively. These findings highlight the variable and stage-specific sensitivity of larval oysters to acidified seawater and the influence that genetic factors have in determining the larval performance of C. gigas exposed to high pCO 2 seawater.

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“…We will refer to them as Baltic M. edulis-like according to Stuckas et al [29]. Adult animals were spawned as described previously, at pH NBS 8.1 and a salinity of 16 psu [14]. Larvae were maintained at GEOMAR at 178C until 48 h post-fertilization (hpf).…”

Section: Animal Collection and Larval Culturementioning

confidence: 99%

In vivo characterization of bivalve larval shells: a confocal Raman microscopy study

Ramesh

Melzner

Griffith

et al. 2018

J. R. Soc. Interface.

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confocal Raman microscopy (CRM), polarized light microscopy and Fourier transform infrared spectroscopy (FTIR) were used to determine if a significant amount of amorphous calcium carbonate (ACC) exists within larval shells of Baltic mytilid mussels (-like) and whether the amount of ACC varies during larval development. No evidence for ACC was found from the onset of shell deposition at 21 h post-fertilization (hpf) until 48 hpf. Larval shells were crystalline from 21 hpf onwards and exhibited CRM and FTIR peaks characteristic of aragonite. Prior to shell deposition at 21 hpf, no evidence for carbonates was observed through CRM. We further analysed the composition of larval shells in three other bivalve species, , and and observed no evidence for ACC, which is in contrast to previous work on the same species. Our findings indicate that larval bivalve shells are composed of crystalline aragonite and we demonstrate that conflicting results are related to sub-optimal measurements and misinterpretation of CRM spectra. Our results demonstrate that the common perception that ACC generally occurs as a stable and abundant precursor during larval bivalve calcification needs to be critically reviewed.

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Mussel larvae modify calcifying fluid carbonate chemistry to promote calcification

Cited by 78 publications

References 43 publications

Expression of calcification‐related ion transporters during blue mussel larval development

Expression of calcification‐related ion transporters during blue mussel larval development

Comparison of larval development in domesticated and naturalized stocks of the Pacific oyster Crassostrea gigas exposed to high pCO2 conditions

In vivo characterization of bivalve larval shells: a confocal Raman microscopy study

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