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    Global assessment of coralline algae mineralogy points to high vulnerability of Southwestern Atlantic reefs and rhodolith beds to ocean acidification

    The data reported in this study expands upon the present knowledge concerning the mineralogy of coralline algae species worldwide, encompassing for the first time coralline algae species data from the Southwest Atlantic Ocean, where this group is the main frame-builders in coral reefs and the major inner component in rhodoliths16,26.Mineralogical analysis revealed that coralline algae species of the Brazilian Shelf were mainly formed of high-Mg calcite. Six coralline algae species in this study had the same range of high-Mg calcite, between 80 and 100%, than the same species from different regions of the world: Lithophyllum corallinae, Lithophyllum kaiseri (as Lithophyllum congestum), Lithophyllum stictaeforme, Lithothamnion crispatum, Melyvonnea erubecens (as Lithothamnion erubecens) and Sporolithon episporum (Table S2). This result confirms that species from different families, such as Corallinaceae, Hapalidiaceae and Sporolithaceae have a CaCO3 skeleton formed mainly of high-Mg calcite.In agreement with earlier studies, the average high-Mg calcite content in Corallinaceae was very similar to the results compiled by Smith et al.11 (96.7 wt.% and 96.2 wt.%, respectively). This pattern was also observed for Hapalidiaceae, which presented a mean value of 88.9 ± 3.6 wt.% in our study and 90.2 wt.%. However, Smith et al.11 registered a high-Mg calcite content of 98 wt.% for Sporolithaceae, while in our study this polymorph had a mean occurrence of 86.2 ± 6.5 wt.%. This percentage can be attributed mainly to the lower content of high-Mg calcite found in Sporolithon yoneshigueae, which is an endemic species of the Brazilian Shelf27.The high similarity between the mineralogy (% high-Mg calcite, % aragonite and % dolomite) of the species belonging to three encrusting algae families, revealed by the cluster analysis, emphasizes the lack of CaCO3 disparities over skeleton mineralogy of coralline algae at family level. This aspect was also evidenced by several studies concerning coralline algae mineralogy11,21,22,23,24,25. This fact was confirmed in the cluster analysis between the mineralogy of the studied coralline species, in which samples from different families were grouped. Considering these findings, the mineralogical pattern exhibited by the crustose algae may not be driven by taxonomic classification, as was first proposed by Chave28. Therefore, the skeletal mineralogy from Brazilian coralline algae species can not be used as a taxonomic character, not even for higher taxonomic levels.In this sense, the mineralogical analysis from L. crispatum, the most common rhodolith-forming species on the Brazilian Shelf16, revealed that samples from the Abrolhos Bank presented higher high-Mg calcite in their composition, and the highest % of Mg substitution in the calcite lattice than the species from the other four regions studied. One of the possible explanations is that the Abrolhos Bank has the highest seawater temperature compared to the other four sites, which influences CCA mineralogy. This result corroborates the hypothesis that coralline algae species do not have a strict control over Mg precipitation as stated by Stanley et al.29. In addition to seawater temperature, Mg/Ca ratio in seawater can also affect the incorporation of magnesium into coralline algae skeletons11,29.In relation to other CaCO3 polymorphs, previous studies have registered some species with up to 20% aragonite11,12. Meanwhile, in this study, S. yoneshigueae presented CaCO3 skeletons formed of more than 30% of aragonite, which expands the range found in coralline algae for this polymorph. The high percentage of aragonite found in S. yoneshigueae could be related to the fact that this species presents larger overgrown calcified empty tetrasporangial compartments, in comparison with other Sporolithaceae species27, which could be filled with aragonite. This feature has mainly been described in the overgrown conceptacles of Lithothamnion sp.30 and in cell infills of Porolithon onkodes31. The presence of aragonite could be also attributed to the use of aragonite granules in the sediment to repair any damage in the alga-substrate attachment32.Raman mapping showed the presence of high-Mg calcite in the bulk of the cell wall with little aragonite in its inner part, which seems to form an inner “shell”, closer to the cell membrane. To date, this is the first study that has utilized Raman maps to show the localization of aragonite in cell walls of coralline algae. The maps consisted of the cellular living layer from the coralline algae crust, right beneath the epithelial cells, which indicates that the mineralization of aragonite occurred in live cells and it was probably not a remineralization process.Aragonite inside cell bodies was first seen by Nash et al.12 using Backscattered Scanning Electron Microscopy. They also reported the presence of dolomite or protodolomite, which were not observed herein by Raman spectroscopy, probably because of the low amount of this polymorph.Previous studies considered that the inclusion of dolomite into carbonate skeletons is a microbial-mediated process after cell death upon the discovery of microbial-associated dolomite formation in anoxic marine33 and freshwater environments34. The presence of several calcium carbonate polymorphs found in coralline algae raises the question of whether all these polymorphs are in fact synthesized by the algae.Indeed, the role of coralline algae in the different forms of calcium carbonate crystal precipitation is a crucial issue that should be addressed. Nowadays, studies calculate the production of CaCO3 by coralline algae based on CCA coverage35, without considering that not all CaCO3 produced in that structure is related to coralline algae biomineralization processes (e.g. secondary calcification processes such as infilling of the older skeleton and skeletal dissolution vs newly deposited carbonate). Therefore, it would be misleading to presume the net CaCO3 accretion of coralline algae structures without knowing the origin of the CaCO3 processes. This is also valid in relation to studies on the influences of atmospheric [CO2] rise on coralline algae, based on weight changes36,37,38 and its impacts on the mineralogy of the existing crust21.Concerning Mg2+ substitution in the high-Mg calcite lattice, we found that Brazilian encrusting algae possess a higher Mg-substitution (46.3% more Mg2+ than the global average) in calcite than specimens collected worldwide. A possible explanation for the higher mean Mg2+ content might be related to the high seawater temperatures39, as this was also observed along the tropical Brazilian Continental Shelf. This can be exemplified by the high Mg2+ content found in fourteen species that occur in warmer waters of the Brazilian Shelf, where the mean surface seawater temperature (SST) ranged between 26.4 and 29.8 °C (from 2008 to 2016), between 17°S and 3°N. The lower Mg2+ amounts presented in L. margaritae and L. attlanticum could also be explained by the temperature, as these species were collected at the southernmost site (27°S) in the temperate zone, where the mean SST (from 2008 to 2016) varied between 22.5 and 25 °C (NOAA Comprehensive Large Array-Data Stewardship System-CLASS: SST50). A relationship between the Mg2+ content and temperature has already been proposed in previous works39 and is widely accepted. Nash and Adey40, when plotting the data collected using XRD, found a very strong correlation coefficient (R2 = 0.975) between mol% MgCO3 in coralline algae and temperature. Moreover, the Mg/Ca rate in coralline algae is used as a proxy archive41 and to generate multicentury-scale climate records from extratropical oceans42.Although seawater temperature is loosely associated with latitude, the New Zealand species, for example, are subjected to lower temperatures (2012 annual maximum and minimum surface seawater temperatures: 21 and 18.7 °C, respectively), while Caribbean and Cocos Island algae grow at higher temperatures (2008–2016 annual maximum and minimum surface seawater temperatures: 29.5 and 23.4 °C, respectively) (NOAA Comprehensive Large Array-Data Stewardship System – CLASS: SST50). If we consider the differences in temperature (≅ 6 °C) and Mg2+ content difference (7.67 wt.%) between the sampling sites along the Brazilian Shelf, we can infer that there is an average increase of 1.27 wt.% of Mg2+ per °C. This value is in the range from 0.4 to 2 wt.% Mg per °C reported previously, both in experimentally and in situ studies39.This relationship between Mg substitution and temperature is also critical in face of the temperature risen episodes that we are seeing all over the world43, including the Brazilian Shelf44. If coralline algae produces High Mg calcite with more Mg substitution in higher seawater temperatures, these thermal anomalies could force the production of a highly soluble polymorph, making coralline algae skeleton even more prone to dissolution.It is well known that high-Mg calcite is the most soluble CaCO3 crystalline polymorph under acidified conditions and that this dissolution is more evident when Mg substitution in the calcite lattice is higher45. In our study 70% of the coralline algae species presented a Mg substitution in the range of 12 to 24% and the mean Mg substitution was 21.1%, which reinforces the susceptibility of Southwestern Atlantic coralline algae to future high [CO2] scenarios.Even though previous experiments using synthetic calcium carbonate showed that the rise of seawater temperature increases Mg substitution, making high-Mg calcite more stable46 and other studies claiming that coralline algae with higher Mg substitution (more than 24% in average) presented less dissolution when exposed to high [CO2]13, Southwestern Ocean coralline algae are already living in a limit situation, where seawater can reach temperatures up to 28 ºC. Since we have a correlation between Mg substitution and temperature around 1.27% Mg per 1 ºC, it would take 2.4 to 6.2 ºC rise so the alga starts to produce a more stable calcite polymorph. Such a temperature rise could be lethal to these algae, also promoting a surface microbial shift that could be crucial to sucectional processes (e.g. settlement) involving other marine organisms, such as corals, which is critical for reef regeneration and recovery from climate-related mortality events47. The comparisons of results obtained through assays with synthetic calcium carbonate must be done with caution, because it should be take into account that the complex calcium carbonate biomineralization processes performed by marine organisms are highly dependent of a narrow range of environmental conditions.In face of the dependency of these environmental conditions, the broad range of Mg content in temperate coralline algae25, a high inter species variability in the % Mg in this study (Abrolhos Bank; 14.5 to 28.8% Mg), as well as an anatomical difference in Mg content in coralline algae40, suggest that other environmental parameters (e.g. Mg/Ca in seawater, light, salinity, etc.) could also drive Mg substitution in coralline algae. Furthemore, coralline algae biological processes might exert some kind of control over Mg-calcite calcification which make them more resilient under rising CO239.Long-term projections of ocean acidification and the CaCO3 saturation state indicated that high-latitude seawater will be undersaturated with respect to high-Mg calcite in the second half of this century45. Early results with coralline algae Sonderophycus capensis and Lithothamnion crispatum in a subtropical mesocosm in Brazil showed that an increase in seawater pCO2 (1000 ppm) enabled both species to continue photosynthesizing but did cause carbonate dissolution48.However, coralline algae from the North Atlantic Ocean, where the temperatures are lower, presented the lowest Mg substitution mean (11.91%), with some algae presenting only 8% of Mg substitution. This fact confers a more stable calcite skeleton to face ocean acidification then individuals from tropical environments. In addition, coralline algae from the Southwestern Atlantic Ocean are already living at temperatures that can be considered a limit for their survival. In fact, for cold water species, a subtle temperature increase could be beneficial in terms of their metabolism, photosynthesis and biomineralization.By the year 2100, surface seawater in all climatic zones could be undersaturated or at metastable equilibrium, with a high-Mg calcite phase containing ≥ 12 mol% Mg45. This could be catastrophic to coralline algae from the Southwest Atlantic Ocean, which produce CaCO3 crystals with more than 20% of Mg substitution in average as shown by the present study and for all the carbonate structures (e.g. rhodolith beds, coralline reefs, etc.) that depends on these skeletons to maintain and grow.It is worth to mention that coralline algae are present since the Mesozoic, in particular Sporolithaceans, which were already abundant in Cretaceous shallow waters49 and have already been submitted to bigger climate change events in the past, such as the Paleocene-Eocene Thermal Maximum (PETM), in which the deep-water temperature increased ∼5 ºC and a massive carbon cycle change took place with a large amount of CO2 absorbed by the oceans50. One of the possible explanations for the survival of coralline algae is that their biomineralogical control is limited to polymorph specification and would be ineffectual in the regulation of skeletal Mg incorporation51. In this sense, in past geological eras, such as the Cretaceous and Paleogene, the Mg/Ca ratio of the oceans favors the precitation of low Mg calcite29,52, which are more stable to dissolution. In a parallel to present day, other fundamental aspect we should take into account is the speed of progression of these changes. Actually, we know that the fast evolution of temperature and acidification present scenarios may result in significant impact on marine biodiversity and in marine calcium carbonate cycle players, as reef organisms and CCA.Carvalho et al.53 proposed that there would be a suitable area for rhodolith occurrence around 230,000 km2, providing a new magnitude to Brazilian Continental Shelf relevance as a major world biofactory of carbonate. In fact, this work confirms the estimation from previous studies, which indicated that this area would correspond to a 2 × 1011 tons of carbonate deposit of the Brazilian coast53. Among the most critical regions in the Brazilian coast, the Abrolhos Bank encompasses the largest continuous latitudinal rhodolith beds registered to date6, which is responsible for the production of approximately 0.025 Gt−1 year−1 of calcium carbonate, similar to those values reported for major tropical reef environments54,55. Another recently described important reef area on the Brazilian Shelf is an extensive carbonate system (≅ 9500 km2) off the Amazon River mouth56, which is composed of mesophotic carbonate reefs and rhodolith beds. These huge carbonate reservoirs and biodiversity hotspots may undergo a major decline if global ocean acidification and temperature rise take place in the near future. More

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    Comparative screening the life-time composition and crystallinity variation in gilthead seabream otoliths Sparus aurata from different marine environments

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    The complete chloroplast genome of critically endangered Chimonobambusa hirtinoda (Poaceae: Chimonobambusa) and phylogenetic analysis

    Assembly and annotation of the chloroplast genomesAssembly resulted in a whole cp genome sequence of C. hirtinoda with a length of 139, 561 bp (Fig. 1), consisting of 83, 166 bp large single-copy region, 20, 811 bp small single-copy regions, and two 21,792 bp IR regions, comprising the typical quadripartite structure of terrestrial plants. The cp genome of C. hirtinoda was annotated with 130 genes, including 85 protein-coding genes, 37 tRNA genes, and 8 rRNA genes (Table 1). Most of the 15 genes in the C. hirtinoda cp genome contain introns. Of these, 13 genes contain one intron (atpF, ndhA, ndhB, petB, petD, rpl2, rpl16, rps16, trnA-UGC, trnI-GAU, trnK-UUU, trnL-UAA, trnV-UAC) and only the gene cyf3 includes two introns, and the gene clpP intron was deleted (Supplementary Table S1). The rps12 gene contained two copies, and the three exons were spliced into a trans-splicing gene18.Figure 1Chloroplast genome map of C. hirtinoda. Different colors represent different functional genes groups. Genes outside the circle indicate counterclockwise transcription, and genes inside the clockwise transcription. The thick black line on the outer circle represents the two IR regions. The GC content is the dark gray area within the ring.Full size imageTable 1 Summary of the chloroplast genome of C. hirtinoda.Full size tableThe accD, ycf1, and ycf2 genes were missing in the cp genome of C. hirtinoda, and the introns in the genes clpP and rpoC1 were lost. This phenomenon is consistent with previous systematic evolutionary studies on the genome structure of plants in the Poaceae family19. The phenomenon of missing genes is reported in other plants20,21,22,23.The total GC content in the C. hirtinoda cp genome was 38.90%, and the content for each of the four bases, A, T, G, and C, was 30.63%, 30.46%, 19.57%, and 19.33%, respectively (Table 2). The LSC region (36.98%) and SSC region (33.21%) exhibited much lower values than the IR region (44.23%), indicating a non-uniform distribution of the base contents in the cp genome, probably because of four rRNAs in the IR region, which in turn makes the GC content higher in the IR region. These values were similar to cp genome results previously reported for some Poaceae plants24,25.Table 2 Base composition in the C. hirtinoda choloroplast genome.Full size tableRepeat sequences and codon analysisSSR consists of 10-bp-long base repeats and is widely used for exploring phylogenetic evolution and genetic diversity analysis26,27,28,29.In total, 48 SSRs were detected in C. hirtinoda, including 27 mononucleotide versions, accounting for 56.25% of the total SSRs, primarily consisting of A or T. Additionally, four dinucleotide repeats consisting of AT/TA and TC/CT repeats, and 3 tri, 13 tetra, and 1penta-repeats (Fig. 2A). From the SSRs distribution perspective, the majority (79%) of SSRs (38) were observed in the LSC area, whereas 6 SSRs in the IR region (13%) and 4 SSRs in the SSC region (8%) were discovered (Fig. 2B). Previous research suggests that the distribution of SSRs numbers in each region and the differences among locations in GC content are related to the expansion or contraction of the IR boundary30.Figure 2Analysis of simple sequence repeats in C. hirtinoda cp genome. (A) The percentage distribution of 45 SSRs in LSC, SSC, and IR regions. (B).Full size imageThe REPuter program revealed that the cp genome of C. hirtinoda was identified with 61 repeats, consisting of 15 palindromic, 19 forward and no reverse and complement repeats (Fig. 3). We noticed that repeat analyses of three Chimonobambusa genus species exhibited 61–65 repeats, with only one reverse in C. hejiangensis. Most of the repeat lengths were between 30 and 100 bp, and the repeat sequences were located in either IR or LSC region31 (Supplementary Table S2).Figure 3Information of chloroplast genome repeats of Chimonobambusa genus species.Full size imageWe identified 20,180 codons in the coding region of C. hirtinoda (Fig. 4, Supplementary Table S3). The codon AUU of Ile was the most used, and the TER of UAG was the least used codon (817 and 19), excluding the termination codons. Leu was the most encoded amino acid (2,170), and TER was the lowest (85). The Relative Synonymous Codon Usage (RSCU) value greater than 1.0 means a codon is used more frequently32. The RSCU values for 31 codons exceeded 1 in the C. hirtinoda cp genome, and of these, the third most frequent codon was A/U with 29 (93.55%), and the frequency of start codons AUG and UGG used demonstrated no bias (RSCU = 1).Figure 4Amino acid frequencies in C. hirtinoda cp genome protein coding sequences. The column diagrams indicate the number of amino acid codes, and the broken line indicates the proportion of amino acid codes.Full size imageComparative analysis of genome structureThe nucleotide variability (Pi) values of the three cp genomes discovered in the Chimonobambusa genus species ranged from 0 to 0.021 with an average value of 0.000544, as demonstrated from DnaSP 5.10 software analysis. Five peaks were observed in the two single-copy regions, and the highest peak was present in the trnT-trnE-trnY region of the LSC region (Fig. 5). The Pi value for LSC and SSC is significantly higher than that of the IR region. In the IR region, highly different sequences were not observed, a highly conserved region. The sequences of these highly variable regions are reported in other plants during examinations for species identification, phylogenetic analysis, and population genetics research33,34,35.Figure 5Sliding window analysis of Chimonobambusa genus complete chloroplast genome sequences. X-axis: position of the midpoint of a window, Y-axis: nucleotide diversity of each window.Full size imageThe structural information for the complete cp genomes among three Chimonobambusa genus species revealed that the sequences in most regions were conserved (Fig. 6). The LSC and SSC regions exhibit a remarkable degree of variation, higher than the IR region, and the non-coding region demonstrates higher variability than the coding region. In the non-coding areas, 7–9 k, 28–30 k, 36 k and other gene loci differed significantly. Genes rpoC2, rps19, ndhJ and other regions differ in the protein-coding region. However, the agreement between the tRNA and rRNA regions is 100%. A similar phenomenon has also been reported by others36.Figure 6Visualization of genome alignment of three species chloroplast genome sequences using Chimonobambusa hejiangensis as reference. The vertical scale shows the percent of identity, ranging from 50 to 100%. The horizontal axis shows the coordinates within the cp genome. Those are some colors represents protein coding, intron, mRNA and conserved non-coding sequence, respectively.Full size imageIR contraction and expansion in the chloroplast genomeDue to the unique circular structure of the cp genome, there are four junctions between the LSC/IRB/SSC/IRA regions. During species evolution, the stability of the two IR regions sequences was ensured by the IR region of the chloroplast genome expanding and contracting to some degree, and this adjustment is the primary reason for chloroplast genome length variation37,38.The variations at IR/SC boundary regions in the three Chimonobambusa genus chloroplast genomes were highly similar in the organization, gene content, and gene order. The size of IR ranges from 21,797 bp (C. tumidissinoda) to 21,835 bp (C. hejiangensis). The ndhH gene spans the SSC/IRa boundary, and this gene extended 181–224 bp into the IRa region for all three Chimonobambusa genus. The gene rps19 was extended from the IRb to the LSC region with a 31–35 bp gap. The rpl12 gene was located in the LSC region of all genomes, varied from 35–36 bp apart from the LSC/IRb (Fig. 7).Figure 7Comparison of LSC, SSC and IR boundaries of chloroplast genomes among the three Chimonobambusa species. The LSC, SSC and IRs regions are represented with different colors. JLB, JSB, JSA and JLA represent the connecting sites between the corresponding regions of the genome, respectively. Genes are showed by boxes.Full size imageThree chloroplast genomes of the Chimonobambusa genus were compared using the Mauve alignment. The results showed that all sequences show perfect synteny conservation with no inversion or rearrangements (Fig. 8).Figure 8The chloroplast genomes of three Chimonobambusa species rearranged by the software MAUVE. Locally collinear blocks (LCBs) are represented by the same color blocks connected by lines. The vertical line indicates the degree of conservatism among position. The small red bar represents rRNA.Full size imagePhylogenetic analysisWe performed a phylogenetic analysis using the complete chloroplast genomes and matK gene reflecting the phylogenetic position of C. hirtinoda. The maximum likelihood (ML) analysis based on the complete chloroplast genomes indicated seven nodes with entirely branch support (100% bootstrap value). However, the three Chimonobambusa genera exhibited a moderate relationship due to fewer samples used, supporting that C. hirtinoda is closely related to C. tumidissinoda with a 62% bootstrap value more than C. hejiangensis. A phylogenetic tree based on the matK gene revealed that Chimonobambusa species clustered in one branch was consistent with the phylogenetic tree constructed by the complete cp genome tree (Fig. 9). The results show that the whole chloroplast genome identified related species better than the former, consistent with the previous study39.Figure 9Maximum likelihood phylogenetic tree based on the complete chloroplast genomes (A) and matK gene (B).Full size image More

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