2017年4月3日，中國海洋大學海洋生命學院包振民教授的研究團隊在Nature子刊Nature Ecology & Evolution上發表題為“Scallop genome provides insights into evolution of bilaterian karyotype and development”的研究文章。2017年11月23日，包老師團隊又在Nature子刊Nature Communication上發文，題為“Scallop genome reveals molecular adaptations tosemi-sessile life and neurotoxins” 。 把小扇貝研究到這種高度、一年發兩篇Nature子刊，可以說很大佬了！

我深居此實驗室數月，仔細研讀文獻，深入接觸文獻的作者們，找到了這兩篇Nature子刊背后的故事。你確定不看看？

1.我可能并不是真的認識扇貝

2

——“扇貝”？不就是“清蒸扇貝”和“蒜蓉扇貝”或者“辣炒扇貝肉”的那個扇貝嘛？！

——對呀！你還知道扇貝的什么知識呢？

——扇貝屬于軟體動物門瓣鰓綱異形亞綱珍珠貝目扇貝科。我國是扇貝的主產國之一，沿海經濟扇貝種類主要有4種，分別是櫛孔扇貝（Chlamys farreri）、海灣扇貝（Argopecten irradians）、蝦夷扇貝（Patinopecten yessoensis）和華貴櫛孔扇貝（Chlamys nobilis）。其中，蝦夷扇貝和海灣扇貝由國外引進。

——那你知道的真不少。

（啪！我就甩過來兩張圖）

常見扇貝（圖片來自海大海洋生物遺傳學與育種教育部重點實驗室）

櫛孔扇貝內部結構（? 海生張）

櫛孔扇貝就是咱們常見、常吃的扇貝啦，清蒸、蒜蓉…… 櫛孔扇貝目前已成為我國海水養殖主要優勢品種之一，在遼寧、河北和山東，尤其是山東沿海已形成相當大的養殖規模。在青島的海鮮市場上很常見。11月這篇發表于Nature Communication上的文章Scallop genome reveals molecular adaptations tosemi-sessile life and neurotoxins研究的就是櫛孔扇貝啦。

而蝦夷扇貝原產于日本、俄羅斯千島群島南部等水域，1982年引入我國山東和遼寧，目前養殖分布在黃渤海，15℃為其最適生長溫度。4月這篇發表于Nature Ecology & Evolution上的文章Scallop genome provides insights into evolution of bilaterian karyotype and development講的就是蝦夷扇貝的故事。

蝦夷扇貝哪里買？青島臺東海鮮市場早市有一家賣，新鮮的34元/斤，不太新鮮的也得30。（筆者連著兩天探訪過清晨五點半的青島臺東一路海鮮市場）

兩種扇貝殼對比（上為蝦夷扇貝，下為櫛孔扇貝。? 海生張）

2.誰說研究扇貝的就只能講扇貝的故事？

——通過扇貝來看生物的宏觀進化

(1)扇貝的基因組是“化石基因組”？

作者們發現扇貝保留了近乎完美的古老染色體核型，是迄今為止發現的最接近雙側對稱動物祖先的染色體核型。扇貝（單倍體染色體數為19）核型較為完美地與科學家們預言的雙側對稱動物祖先（單倍體染色體數17）核型（Simakov, O. et al. Insights into bilaterian evolution from three spiralian genomes. Nature 493, 526–531 (2013)）相符合。而這個“化石基因組”對于研究雙側對稱生物演化有著重要的意義。扇貝基因組，一把通向未知世界的神奇的鑰匙 。

The outstanding preservation of ancestral bilateriankaryotype in the scallop genome. Chromosome-based macrosynteny is shown in theform of dot plots with comparisons between the chromosomes of 12 bilateriangenomes (x axis) and the 17 presumed bilaterian ALGs (ALG1–17, y axis)that were previously reconstructed5.The scallop genome anchored in 19 chromosomes shows the highest level ofchromosome preservation (conservation index (CI) = 0.81) that far exceeds those of other bilaterians (CI = 0–0.42) withchromosome-level assemblies, suggesting that the scallop has a karyotypeclosely resembling that of a bilaterian ancestor. The haploid chromosome number(n) is shown for each species, and the CI measures the extent ofpreservation of bilaterian ALGs in each species. The chromosome-anchored genomeassemblies of Pacific oyster (C. gigas) and pearl oyster (P. fucata)were generated in this study by using two recently published high-densitylinkage maps

（2）Hox表達調控的新模式？

作者們發現扇貝基因組保留了最完整的Hox和ParaHox基因簇，提出了雙側對稱動物Hox基因簇分段共線性（STC）表達新模式，闡明了動物體制發生決定基因Hox基因簇表達的起源和演化途徑。

a, Chromosomal organization of Hox and ParaHox genesof scallop and other lophotrochozoans. Unlike other lophotrochozoans whose Hoxand ParaHox clusters are usually fragmented, both clusters arepresent as single, intact clusters in scallop, possibly representing theancestral state of these clusters in the lophotrochozoan ancestor (top).Horizontal arrows and triangles denote transcription orientation and externalgene insertion, respectively.

c, Temporal expression of scallop Hox and ParaHox clustergenes. Expression of ParaHox cluster follows temporal co-linearityduring embryonic and larval stages, whereas expression of Hox clusterexhibits an STC for four subclusters (S1: Hox1–Hox3, S2: Hox4–Hox5,S3: Lox5–Lox2, S4: Post2–Post1), with leading genesgenerally activated earlier than their followers in each subcluster. Verticalthick arrows indicate co-activation of leading genes of four subclusters,whereas thin arrows indicate gene activation order within each subcluster orthe whole cluster. 2-8cell, 2–8 cells; Bla, blastula; Gas, gastrula; Tro,trochophore; Dst, D-stage larva; Ped, pediveliger; Juv, juvenile.

d, Spatially co-linear expression of four leading genes (Hox1,Hox4, Lox5, Post2) of each subcluster at the gastrulastage. The expression regions of four leading genes almost span the entireanterior–posterior body axis, suggesting the prominent roles of these leadinggenes in early body plan determination. Expression of other Hox genes isnot detectable at this stage (see Supplementary Fig. 23) except Lox4,which is less likely to be a candidate leading gene as its expression does notconform to the characteristic pattern of leading genes (stronger expression atearly developmental stages than latter stages). A, anterior; P, posterior; V,ventral; D, dorsal. Scale bar, 50 μm.

Schematic illustration ofvarious types of Hox temporal expression andtheir possible evolutionary origins. The phenomenon of STC exists in an intact Hoxcluster of scallop and fragmented clusters of different lophotrochozoanlineages (bivalves and annelids)9,29 anddistantly related bilaterian groups (ecdysozoan and deuterostome)30,31, suggesting that STC could be ancestral. Thebasal bilaterian acoels33 have only threeunlinked Hox genes (corresponding to Hox1, Hox4/5 and Postparalogous group46), and it has beenproposed that these acoel Hox genes may belong to the ancient Hox clusterof Urbilateria or proto-Urbilateria, duplication of which gives rise to presentprotostome/deuterostome Hox clusters46.In the acoel Convolutriloba longifissura, all three Hox genesshow contemporaneous expression after gastrulation32,which is consistent with the co-activation of subclusters in scallop and otherbilaterians, and suggests STC might be established along with the stepwiseduplication of primordial Hox genes. Interestingly, the Hox expressionof the annelid C. teleta exhibits an unusual mode of WTC that issubcluster-based35 (called S-WTC here),probably representing an intermediate state in evolutionary transition betweenSTC and WTC. STC may be central to the bilaterian body plan evolution and, ifindeed ancestral, would provide bilaterian ancestors great potential ingenerating diverse body plans.

3.做扇貝，還是要探究一些扇貝的生物學問題的

——看看扇貝的微觀進化

3

（1）扇貝眼睛的遺傳調控及進化起源

Summary of opsins and Pax genes used in cephalic andnoncephalic bilaterian eyes or light sensors from this and previous studies.The observation of cephalic and noncephalic bilaterian eyes controlled by different Pax regulators (Pax6 for the former and Pax2/5/8 for the latter) across majorbilaterian clades, supporting their different evolutionary origins.

研究發現扇貝眼睛的發生是由Pax2/5/8主導，向之前普遍認為眼睛起源單源論(以Pax6基因主導)提出了挑戰。頭眼（人類、果蠅等）由Pax6主導，而扇貝、線蟲的軀干眼由Pax2/5/8主導。

Diversity of opsins andphototransduction cascades in scallop eyes.

a, Scallop has numerous noncephalic eyes scattered along mantlemargins, with two distinct retinal layers consisted of rhabdomeric and ciliaryPRCs, respectively (scale bars on the upper and lower images represent 5 cm and100 μm, respectively). Diverse opsin types (r-opsin, Go-opsin and c-opsin) are identified in the scallopgenome, with r-opsins showing the highest expression and probably playing aprominent role in scallop eye function. The finding of c-opsin expression inscallop eyes is intriguing, as c-opsin has not been identified in scallopsbefore and was once considered a vertebrate-type opsin for ciliaryphototranduction. Eye samples from three individuals were used in expressionevaluation with standard errors shown for eye and mantle groups.

b, Key components of different phototransduction cascades(mediated by r-opsin, Go-opsin and c-opsin)identified in the scallop genome with their gene expression in eyes relative tomantle colour-coded. The coexistence of multiple phototransduction cascades inscallop eyes is unusual and intriguing, as these cascades have been selectivelypreserved for visual function in invertebrates (r-opsin) and vertebrates(c-opsin). FC, fold change.

上圖示研究發現的扇貝眼睛的多套光傳導通路（分別由r-opsin、Go-opsin和c-opsin主導）及視蛋白進化分析。

（2）貝類毒素積累及耐受機制

Toxinresistance and response regulatory networks in the scallop kidney andhepatopancreas.

a Aminoacids conferring PST or TTX resistance on sodium channel Nav1 (highlighted inred) identified inthis and other studies. Skull signs indicate toxin-producing and -resistantspecies.

b Expressionof sodium channels Nav1 and Nav2, and PST concentration and toxicity levels inmajor organs of C. farreri. Toxicity (μgSTX eq. per 100 g) was determined by converting total concentration of PSTs tomicrograms of STX equivalents per 100 g of tissue.

c Temporalvariations in abundance of different PSTs and gene networks in the kidney andhepatopancreas after exposure to the toxic alga Alexandrium minutum. Toxin response modules were identified by enrichment analysis of DEGs duringexposure to A. minutum and eachmodule was annotated with the two most significantly enriched GO term(s). The green moduleis the largest kidney-specificresponse module, where cytosolic sulfotransferase (Sult) genes are enriched andhighly expressed on day 5 after A. minutum exposure (as indicated in the heatmap).

d Aschematic diagram showing different roles of the scallop hepatopancreas andkidney in toxin metabolism, with the hepatopancreas primarily responsible forPST accumulation, whereas the kidney primarily for PST transformation mediatedby SULTs.

作者們探究了扇貝對麻痹性貝毒（PST）積累、轉化及耐受的組學基礎，確定腎臟是扇貝毒素轉化的主要器官，解析了PST攻毒過程中扇貝的基因網絡調控及表達模式，提出了扇貝貝毒耐受及轉化的遺傳機制。

所以以后吃扇貝的時候，請先把毒素含量最高的肝胰腺（黑色一坨）和腎臟（兩顆小黃豆狀）剔除再吃吧！

（3）扇貝足絲組成及黏附機制

The evolution of opsin diversity and photoreceptiontuning in C. farreri.

a. Morphology of scallop eyes scattered along the edge ofmantles (left, scale bar: 1 cm), schematic structure of a typical scallop eye(middle), and expression of diverse opsin genes in scallop eyes (right). Eyesamples from three individuals were used in expression evaluation with standarderror shown for eye and mantle groups. The asterisks indicate genes showingsignificantly higher expression in eyes than in the mantle (p-value< 0.05, the exact test by edgeR).

b. R-opsin gene structures of Mollusca and Branchiopoda.Exons rather than introns were plotted in proportion, with scale barrepresenting 500 bp. NETR (neurotrypsin) and FPV246 (putative ankyrin repeatprotein) are the conserved neighboring genes.

c. Sequence similarity and Ka/Ks values of all opsingenes between the scallops of C. farreri (CF)and P. yessoensis (PY). These datawere calculated based on full protein sequences. The black line insides the boxindicates the median value, and the whiskers extend from the first or third quartiles to the minimum or maximum values.

d. Bivalve opsin phylogeny and variation at keyfunctional sites sensitive to various light ranges. Species abbreviations: Chlamys farreri (CF), Pinctada fucata (PF), Crassostrea gigas (CG), Argopecten irradians (AI), Patinopecten caurinus (PC) and Argopecten purpuratus (AP). Sitecombinations of “SFA” “GFA” and “AFA” above the major branches are the putativeancestral bivalve types deduced from extant species. Colors of the sitescorrespond to the colors or wavelengths of opsin sensitivity in human opsins

研究查明了扇貝足絲顯微結構及蛋白關鍵組分，確定了酪氨酸酶、磷酸化酶等酶類參與的催化反應對足絲粘附起重要作用。海洋生物黏附材料？聽起來就很有應用前景呢！

4.文章背后的故事？我們學到了什么樣的科研精神？

4

4

合作。這兩篇文章都不是以一人之力、一實驗室之力完成。攻克一個科學難題，可能需要來自不同學校/科研機構、不同研究方向的科研工作者們的群策群力。

自信。“我一個做水產育種的為啥不能發表最頂級的文章？！” 這種自信不是盲目自大，而是在實驗室老師們經歷多次失敗后成長
起來的。

努力。看起來是包老師團隊在一年內發表了這兩篇文章，可是這兩篇文章的工作花了整個科研團隊好幾年的時間，可謂厚積薄發！

向研究人員們致敬！

此外，海生張最近正在煙臺市某育苗場從事扇貝育種工作，請看他從生產一線發來的照片。

這么大的蝦夷扇貝我可是第一次見

美麗的海灣扇貝

扇貝銷魂的泳姿

后續會推出《小師弟下場日記》，我們一起走進扇貝育種場，去看看我們餐桌上營養而美味的扇貝是怎么長大的。敬請期待!

征稿啟事

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