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Polysaccharides─Important Constituents of Ice-Nucleating Particles of Marine Origin
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Occurrence, Fate, and Transport of Contaminants in Indoor Air and Atmosphere
室内空气与大气中污染物的存在、归趋及迁移

Polysaccharides─Important Constituents of Ice-Nucleating Particles of Marine Origin
多糖类——海洋源冰核粒子的重要组分
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Environmental Science & Technology

Cite this: Environ. Sci. Technol. 2025, 59, 10, 5098–5108
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https://doi.org/10.1021/acs.est.4c08014
Published March 7, 2025

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Abstract  摘要

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Remote marine regions are characterized by a high degree of cloud cover that greatly impacts Earth’s radiative budget. It is highly relevant for climate projections to represent the ice formation in these clouds. Therefore, it is crucial to understand the sources of ice-nucleating particles (INPs) that enable primary ice formation. Here, we report polysaccharides produced by four different aquatic eukaryotic microorganisms (Thraustochytrium striatum, Tausonia pullulans, Naganishia diffluens, Penicillium chrysogenum) as responsible ice-nucleating macromolecules (INMs) in these samples originating from the marine biosphere. By deriving a classical nucleation theory-based parametrization of these polysaccharidic INMs and applying it to global model simulations, a comparison to currently available marine atmospheric INP observations demonstrates a 44% contribution of polysaccharides to the total INPs of marine origin within −15 to −20 °C. The results highlight the relevance of biological INMs as part of the INP population in remote marine regions.
偏远海域以高云量为特征,这对地球辐射收支具有重大影响。准确表征这些云层中的冰晶形成过程对气候预测极为重要。因此,理解促成初始冰晶形成的冰核粒子(INPs)来源至关重要。本研究首次报道了四种不同水生真核微生物(裂殖壶菌、普鲁兰陶松菌、流散长孢酵母、产黄青霉)产生的多糖作为海洋生物圈样本中具有冰核活性的生物大分子(INMs)。通过建立基于经典成核理论的多糖类 INMs 参数化方案,并将其应用于全球模型模拟,与现有海洋大气 INP 观测数据的对比表明,在-15 至-20°C 温度区间内,多糖对海洋源 INPs 总量的贡献率达 44%。研究结果凸显了生物源 INMs 作为偏远海域 INP 群体组成部分的重要性。

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Synopsis  摘要

The ability of aquatic fungi and protists to form ice is caused by polysaccharides. In the remote marine atmosphere, these macromolecules can be as important as mineral dust ice-nucleating particles in the temperature range relevant for mixed-phase clouds.
水生真菌和原生生物形成冰的能力是由多糖引起的。在远洋大气中,这些大分子在与混合相云相关的温度范围内,其重要性可与矿物尘埃冰核粒子相媲美。

1. Introduction  1. 引言

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Ice-nucleating particles (INPs) initiate the formation of ice crystals in clouds and consequently impact the radiative balance of the Earth’s atmosphere and precipitation formation and are relevant for understanding climate sensitivities. (1) For large parts of the remote oceans, particularly the Southern Ocean where INP concentrations are low, (2,3) discrepant observations exist in the representation of cloud phase, driven by strong biases in the radiative effect variables of atmospheric models. (4) A better understanding of INP sources, such as mineral dust or sea spray aerosol (SSA), (5−7) INP transport and underlying mechanisms of ice nucleation at the molecular level offer a large potential to improve climate modeling, especially for the sensitive, but still quite unexplored climate hot spots, such as the Southern Ocean and the Arctic. (8−13) In general, the ocean is known to be a source of INPs because it contains ice-active microorganisms (and parts or products thereof) that can enter the atmosphere as part of SSA. (6,14−19) Increased biological activity of ocean water for example during a phytoplankton bloom thus provides a larger reservoir for INPs that can be aerosolized. (6,15−17,20−23) Indications have been found that organic compounds produced from marine microorganisms may be responsible for the observed ice-nucleating ability (15−17,24) and can be enriched in the ocean surface microlayer. (15,25−28) Various marine microorganisms have been investigated and found to be active in nucleating ice, including bacteria, (16,29−33) algae, (14,33−35) marine diatoms, (29,32,33,36−39) haloarchaea, (40) viruses, (41) and fungi. (31,42) Alongside algae and bacteria as primary contributors to biomass production and degradation, marine fungi are now gaining recognition for their significant role in the carbon cycle. (43,44) However, significant knowledge gaps remain regarding the geographical and annual distribution of fungi and pseudofungi. These organisms are underrepresented in environmental surveys due to their absence from databases, (45) and their potential role as INPs remains largely unexplored. The latter is the subject of this study.
冰核颗粒(INPs)能够引发云中冰晶的形成,进而影响地球大气的辐射平衡和降水形成,对理解气候敏感性具有重要意义。(1) 在偏远海域的大部分区域,特别是 INP 浓度较低的南大洋,(2,3) 由于大气模式辐射效应变量的强烈偏差,云相态的观测数据存在显著差异。(4) 通过更好地理解 INP 来源(如矿物粉尘或海浪气溶胶 SSA)(5−7)、INP 传输以及分子尺度上的冰核形成机制,将极大提升气候模拟能力——这对南大洋和北极等敏感却仍待探索的气候热点区域尤为重要。(8−13) 通常认为海洋是 INPs 的来源之一,因其含有冰活性微生物(及其组分或代谢产物),这些物质可通过 SSA 进入大气。(6,14−19) 例如在藻华期间,海水生物活性的增强会为可气溶胶化的 INPs 提供更丰富的储备。 (6,15−17,20−23)已有迹象表明,海洋微生物产生的有机化合物可能是观测到冰核活性的原因(15−17,24),并且这些物质会在海洋表面微层中富集。(15,25−28)多种海洋微生物已被证实具有冰核活性,包括细菌(16,29−33)、藻类(14,33−35)、海洋硅藻(29,32,33,36−39)、嗜盐古菌(40)、病毒(41)和真菌(31,42)。虽然藻类和细菌作为生物量生产与降解的主要贡献者,但海洋真菌在碳循环中的重要作用正逐渐被认识。(43,44)然而,关于真菌和假真菌的地理分布与年度变化仍存在显著认知空白。由于数据库缺失导致环境调查中这些生物的代表性不足(45),其作为冰核粒子的潜在作用也基本未被探索。后者正是本研究的主题。
Ice-nucleating macromolecules (INMs) cause the activity of biogenic INPs. (46) While the ice-nucleating activity (INA) of terrestrial microorganisms and pollen have been attributed to specific proteins or polysaccharides, respectively, (47−51) little is known about the chemical identity of biogenic marine INMs from SSA to date. Studying planktonic microorganisms, Wolf et al. (52) found strong evidence that proteinaceous and saccharidic components determine the INA of organics in SSA. Alpert et al. (24) found proteins and polysaccharides in both ambient and laboratory-generated INPs containing exudates from planktonic microbes. Further, a polysaccharidic nature of marine INMs appears plausible based on correlations between INA and free glucose, a non-ice-active monosaccharide and degradation product of polysaccharides, found in the Arctic surface seawater. (53) To identify and quantify the contribution of specific ice nucleation active components to marine INP population, targeted measurements of the chemical compounds are required. (16,17)
冰核大分子(INMs)是生物源冰核颗粒(INPs)活性的关键因素。(46) 尽管陆地微生物和花粉的冰核活性(INA)已分别被归因于特定蛋白质或多糖(47−51),但迄今为止对源自海盐气溶胶(SSA)的生物源海洋 INMs 的化学特性仍知之甚少。Wolf 等人(52)在研究浮游微生物时发现有力证据,表明蛋白质和糖类成分决定了 SSA 中有机物的 INA。Alpert 等人(24)在含浮游微生物分泌物的环境及实验室生成的 INPs 中均检测到蛋白质和多糖。此外,根据北极表层海水中 INA 与非冰活性单糖(多糖降解产物)游离葡萄糖的相关性,海洋 INMs 可能具有多糖特性(53)。为识别和量化特定冰核活性成分对海洋 INP 群体的贡献,需开展针对这些化学物质的定向测量(16,17)。
For high predictability modeling of atmospheric INP concentrations over remote marine regions, two main INP sources are commonly taken into account: mineral dust and marine organics derived from SSA. (54−56) Therefore, state-of-the-art INP parametrizations are applied which either consider unspecified INP concentrations or use bulk aerosol properties as proxies such as number, surface area, or broad categories of aerosol constituents (e.g., mineral dust, sea salt). (8,57−59) In doing so, mostly a log-linear or polynomial relationship between INP concentration and temperature is assumed. (15,57,59−62) Although this approach generally reflects the observed temperature-dependent INP concentrations, extrapolating to a wider temperature range than supported by observations is not necessarily valid and lacks a physical basis. Furthermore, apart from mineral dust, the INP concentration is therefore usually estimated only by indirect proxies, i.e., not directly based on the presumably different chemical aerosol components that actually cause the freezing in different temperature regimes. For mineral dust, different ice-nucleating components are accounted for already. (4,63)
为对偏远海域大气冰核颗粒(INP)浓度进行高预测性建模,通常需考虑两大主要来源:矿物尘埃和源自海盐气溶胶(SSA)的海洋有机物。(54−56)因此,当前最先进的 INP 参数化方案主要采用两种方法:或考虑未分类的 INP 浓度,或使用气溶胶整体特性(如数量、表面积或气溶胶成分大类,例如矿物尘埃、海盐等)作为代用指标。(8,57−59)在此过程中,通常假设 INP 浓度与温度之间存在对数线性或多项式关系。(15,57,59−62)虽然这种方法总体上能反映观测到的温度依赖性 INP 浓度,但将观测范围外推至更宽温度区间未必有效且缺乏物理基础。此外,除矿物尘埃外,INP 浓度通常仅通过间接代用指标估算,即并非直接基于实际引发不同温区冻结的、可能具有化学差异的气溶胶组分。目前仅对矿物尘埃已考虑其不同冰核活性组分。(4,63)
In this study, we investigate the ice nucleation activity of marine polysaccharides derived from marine fungi and protists as well as from commercially available standard polysaccharides. We develop a physically based parametrization and integrate these findings together with mineral dust INPs in a global model to assess their relevance by comparing with available atmospheric INP observations in marine regions.
本研究探究了源自海洋真菌和原生生物的商业化标准多糖的冰核活性。我们建立了基于物理过程的参数化方案,并将这些发现与矿物粉尘冰核颗粒整合到全球模型中,通过对比现有海洋区域大气冰核观测数据来评估其重要性。

2. Experimental Methods  2. 实验方法

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2.1. Isolation and Cultivation of Microorganisms
2.1 微生物分离与培养

The abundance of nonphototrophic microorganisms was determined in the marine environment by extracting and sequencing DNA collected during a cruise on the R/V Helmer Hanssen near Svalbard in November 2017 in different environmental compartments including airborne and surface water samples (Table S1, Figure S1, and details described in the Supporting Information (SI)). Microorganisms from various environments, including nearshore Arctic sediment in Tromsø and Arctic marine plankton, were sampled, focusing on heterotrophic eukaryotic microbes such as fungi and a protist. The collected samples were cultivated for further analysis (see Table S2, SI). Specifically, we studied one thraustochytrid (Thraustochytrium striatum), two yeasts (Tausonia pullulans and Naganishia diffluens), and one filamentous fungus (Penicillium chrysogenum).
通过提取并测序 2017 年 11 月在斯瓦尔巴群岛附近 R/V Helmer Hanssen 科考船上采集的不同环境区室(包括空气传播和表层水样本)中的 DNA,测定了海洋环境中非光合微生物的丰度(表 S1、图 S1 及支持信息(SI)中的详细描述)。从包括特罗姆瑟近岸北极沉积物和北极海洋浮游生物在内的多种环境中采样微生物,重点关注真菌和原生生物等异养真核微生物。采集的样本经过培养以进行后续分析(见表 S2,SI)。具体而言,我们研究了一种破囊壶菌(裂殖壶菌 Thraustochytrium striatum)、两种酵母(出芽短梗霉 Tausonia pullulans 和流散长孢酵母 Naganishia diffluens)以及一种丝状真菌(产黄青霉 Penicillium chrysogenum)。

2.2. Microphysical and Chemical Analyses
2.2 微物理与化学分析

The ice nucleation activity of these cultivated fungi and thraustochytrids was analyzed using a droplet freezing assay (Section S4 SI). To constrain potential candidates for ice-nucleating macromolecules produced by these microbes different physical and chemical pretests were done including a 0.2 μm membrane filtration, (15,17,64) heat treatment (95 °C for 1 h), (65,66) and CaCl2 precipitation (1.6 g L–1 CaCl2 added to 0.2 μm filtered aliquots of T. pullulans). To confirm the preliminary observations in the microbial samples, the following commercially available standard polysaccharides were also analyzed: laminarin, λ-carrageenan, κ-carrageenan, alginic acid (long- and short-chained), agar, cellulose, xanthan gum, and a lipopolysaccharide from P. aeruginosa. The total combined carbohydrates (TCCHO, i.e., hydrolyzable polysaccharide) content and monosaccharide composition was quantified after an acid hydrolysis (0.8 M HCl, 100 °C, 20 h) using a high-performance anion-exchange chromatography with pulsed amperometric detection (67) as described in detail in the SI. For the determination of total organic carbon (TOC), 20 μL of the liquid culture samples were pipetted on a rectangular punch (1.5 cm2) of quartz fiber filter, dried up for 20 min at room temperature, and analyzed on the Lab OC-EC analyzer (Sunset Laboratory Inc., USA) applying the standard temperature protocol EUSAAR2.91.
采用液滴冻结实验分析了这些培养真菌和破囊壶菌的冰核活性(详见 SI 第 S4 节)。为确定这些微生物产生的潜在冰核大分子候选物,进行了不同物理化学预处理测试,包括 0.2 μm 膜过滤(15,17,64)、热处理(95°C 持续 1 小时)(65,66)以及 CaCl2 沉淀(向出芽短梗霉 0.2 μm 过滤液中添加 1.6 g L–1 CaCl2)。为验证微生物样本的初步观察结果,还分析了以下市售标准多糖:昆布多糖、λ-卡拉胶、κ-卡拉胶、海藻酸(长链与短链)、琼脂、纤维素、黄原胶以及铜绿假单胞菌脂多糖。通过酸水解(0.8 M HCl,100°C,20 小时)后,采用高效阴离子交换色谱-脉冲安培检测法(67)对总碳水化合物(TCCHO,即可水解多糖)含量及单糖组成进行定量分析,具体方法详见 SI。 为测定总有机碳(TOC)含量,取 20 微升液体培养样品滴加于 1.5 平方厘米的石英纤维滤膜上,室温干燥 20 分钟后,采用美国 Sunset 实验室生产的 Lab OC-EC 分析仪,按照 EUSAAR2.91 标准温度程序进行分析。

2.3. Application of INP Parametrization to Global Model Simulations
2.3. 冰核粒子参数化在全球模型模拟中的应用

Existing simulation data for the year 2010 (68) that was generated with the atmospheric chemistry transport model TM5 (69) was used in the present study. The data set was chosen as it provides the necessary proxy mineral dust and sea salt for calculating INP concentrations and a high time resolution (hourly). From the simulation, the mass concentration of sea salt and mineral dust as well as the number concentrations in the soluble and insoluble accumulation and coarse modes were used to derive INP concentrations. For INPs from mineral dust, the parametrization by Niedermeier et al. (2015, N15) (70) was used. INPs from marine polysaccharides are calculated by applying the parametrization derived in this work (HSZ25). A dynamic emission modeling of polysaccharides and, hence, the aerosol polysaccharide content is beyond the scope of this study. Therefore, it is assumed that a constant percentage of 0.5 and 0.1% of the sea salt mass in the soluble accumulation and coarse mode, respectively, consists of marine polysaccharides. This polysaccharide fraction in SSA is derived from ambient measurements conducted during the PI-ICE campaign in the Southern Ocean (0.2–0.5% in accumulation mode, 0.03–0.05% in coarse mode, campaign mean in the respective size bins of the size-resolved impactor data), (67) the PASCAL campaign in the central Arctic Ocean (0.1–0.9% in accumulation mode, 0.1–0.7% in coarse mode, campaign mean in the respective size bins of the size-resolved impactor data), (71) on Cape Verde (0.1% campaign mean in PM10), (72) and at Mt. Zeppelin, Svalbard, Norway (0.4% campaign mean in PM1). (73) Despite the limited data basis of polysaccharide measurements, the range of single measurements as well as the mean polysaccharide content in SSA seems to be similar between the Arctic and Southern Ocean. To estimate the uncertainty caused by this assumption, a lower and upper bound for the polysaccharide content of 0.05 and 0.5%, respectively, in both accumulation and coarse mode was used as well. By applying a mass fraction, co-emission of sea salt and marine organic aerosol is directly reflected. Hence, uncertainties from modeling, estimating concentrations of organics or biological activity in the sea surface microlayer, and enrichment factors during aerosolization are avoided. On the other hand, the spatiotemporal variability of the polysaccharide concentrations in aerosol and more detailed emission descriptions cannot be easily considered at present. For comparison to our polysaccharide-based INP parametrization (HSZ25), the INP parametrization of McCluskey et al. (2018, M18) (59) is applied, representing an estimate of nonheat-labile marine INPs in sea spray aerosol, hence, originating from seawater, and by purpose avoiding any influence of mineral dust. INP concentrations were calculated for the hourly model data and averaged over the whole year. The modeled INP concentrations were evaluated against observational data sets from remote marine regions covering more than a decade. Campaigns in the Southern Ocean provided the largest share of observations, but also the Arctic Ocean, as well as Northern and Tropical Atlantic and Pacific, are represented. By using the annual average INP concentration, the effects of the short-term variability of mineral dust concentrations in the Southern Ocean region are avoided. As both the modeled mineral dust and sea salt concentrations in the Southern Ocean do not show an obvious seasonal cycle (see also the SI), we assume that derived annual average INP concentrations in such remote marine regions are similar in different years. Further, the main conclusions are drawn from the comparison of HSZ25 and M18 that use the same proxy, i.e., the modeled sea salt concentration, hence both parametrizations would have the same deviations from the exact conditions during the individual measurement periods. The HSZ25 parametrization is evaluated against M18 in terms of improved agreement of modeled and observed INP concentrations within a factor of 10 (FAC10). This refers to the increase in FAC10 in addition to mineral dust INPs only. The fraction of improved agreement within a factor of 10 explained by polysaccharides FHSZ25, M18 (right column in Table S5) is calculated as
本研究采用了 2010 年大气化学传输模型 TM5 生成的现有模拟数据。选择该数据集是因为其能提供计算冰核粒子浓度所需的矿物尘和海盐替代指标,并具有高时间分辨率(每小时)。通过模拟数据,利用海盐与矿物尘的质量浓度、以及可溶性与不可溶性累积模态和粗模态中的数浓度来推导冰核粒子浓度。对于矿物尘来源的冰核粒子,采用了 Niedermeier 等人(2015,N15)提出的参数化方案。海洋多糖类冰核粒子的计算则应用了本工作推导的参数化方案(HSZ25)。多糖物质的动态排放建模及其气溶胶多糖含量不在本研究范围内,因此假设可溶累积模态和粗模态中海盐质量分别恒定含有 0.5%和 0.1%的海洋多糖成分。 海盐气溶胶(SSA)中的多糖组分源自以下环境观测数据:南大洋 PI-ICE 航次(积聚模态 0.2-0.5%、粗粒子模态 0.03-0.05%,为粒径分级撞击器数据各粒径区间的航次均值)(67)、北冰洋中部 PASCAL 航次(积聚模态 0.1-0.9%、粗粒子模态 0.1-0.7%,为粒径分级撞击器数据各粒径区间的航次均值)(71)、佛得角(PM10 中航次均值 0.1%)(72)以及挪威斯瓦尔巴群岛齐柏林山(PM1 中航次均值 0.4%)(73)。尽管现有多糖测量数据有限,但北极与南大洋的单次测量值范围及 SSA 中多糖平均含量似乎较为接近。为评估该假设带来的不确定性,同时采用积聚模态和粗粒子模态中多糖含量 0.05%与 0.5%分别作为下限和上限。通过应用质量分数,直接反映了海盐与海洋有机气溶胶的共排放特征。 因此,避免了来自建模、估算海面微表层有机物浓度或生物活性以及气溶胶化过程中富集因子的不确定性。另一方面,目前尚难以轻易考虑气溶胶中多糖浓度的时空变异性以及更详细的排放描述。为与我们基于多糖的冰核粒子参数化方案(HSZ25)进行比较,采用了 McCluskey 等人(2018 年,M18)(59)的冰核粒子参数化方案,该方案代表了对海喷雾气溶胶中非热不稳定海洋冰核粒子的估算,因此源自海水,并有意避免矿物粉尘的任何影响。冰核粒子浓度是根据每小时模型数据计算并全年平均得出的。模拟的冰核粒子浓度与覆盖十多年的偏远海洋区域观测数据集进行了评估。南大洋的观测活动提供了最大份额的数据,但北冰洋以及北大西洋、热带大西洋和太平洋也有代表性数据。 通过采用年平均冰核粒子(INP)浓度,可避免南大洋区域矿物尘浓度短期波动的影响。由于南大洋模拟的矿物尘与海盐浓度均未呈现明显季节性周期(参见补充信息),我们推断此类偏远海域的年平均 INP 浓度在不同年份间具有相似性。此外,主要结论源自 HSZ25 与 M18 两种参数化方案的对比——二者均采用模拟海盐浓度作为代理指标,因此在各测量时段内与真实条件的偏差程度相同。相较于 M18 方案,HSZ25 参数化的评估标准在于将模拟与观测 INP 浓度的吻合度提升至 10 倍误差范围内(FAC10)。该指标特指在仅考虑矿物尘 INPs 基础上实现的 FAC10 提升幅度。表 S5 右栏所列的多糖贡献率 FHSZ25,M18,即用于量化在 10 倍误差范围内吻合度改善中可归因于多糖作用的比例,其计算公式为:
FHSZ25,M18=FAC10N15+HSZ25FAC10N15FAC10N15+M18FAC10N15
(1)
where FAC10N15 is the agreement against the observations within a factor of 10 when using only mineral dust INPs (according to N15). Accordingly, FAC10N15+M18 is that agreement when using the combination of N15 with marine INPs derived from sea spray aerosol according to M18, and FAC10N15+HSZ25 when using the combination of N15 with marine polysaccharide INPs.
其中 FAC10N15 表示仅使用矿物粉尘冰核颗粒(依据 N15)时,观测值在 10 倍范围内的吻合度。相应地,FAC10N15+M18 表示采用 N15 与 M18 提出的海盐气溶胶来源海洋冰核颗粒组合时的吻合度,而 FAC10N15+HSZ25 则表示采用 N15 与海洋多糖冰核颗粒组合时的吻合度。

2.4. Data and Code Availability
2.4. 数据与代码获取

Sequence results of eukaryotic microorganisms are available https://www.ncbi.nlm.nih.gov with the respective accession numbers given in Table S2. Sequence abundance of airborne and aquatic microorganisms sampled in November 2017 on R/V Helmer Hanssen, and INM concentrations of different microorganisms, polysaccharides, and targeted tests can be found on 10.5281/zenodo.10421589. Data on combined carbohydrates and inorganic ions in size-resolved ambient aerosol particles during PI-ICE (Southern Ocean) and Cape Verde can be accessed at https://doi.pangaea.de/10.1594/PANGAEA.927565 and https://doi.pangaea.de/10.1594/PANGAEA.969080, respectively. The applied codes are available on 10.5281/zenodo.10423597.
真核微生物的测序结果可在 https://www.ncbi.nlm.nih.gov 查询,对应登录号详见表 S2。2017 年 11 月在 R/V Helmer Hanssen 科考船上采集的空气和水生微生物序列丰度数据、不同微生物的冰核活性浓度、多糖含量及目标测试结果可通过 10.5281/zenodo.10421589 获取。PI-ICE(南大洋)和佛得角航次中分级环境气溶胶颗粒的复合碳水化合物与无机离子数据分别存储于 https://doi.pangaea.de/10.1594/PANGAEA.927565 和 https://doi.pangaea.de/10.1594/PANGAEA.969080。应用代码存放于 10.5281/zenodo.10423597。

3. Results and Discussion
3. 结果与讨论

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3.1. Polysaccharides Responsible for INA of Marine Eukaryotic Microorganisms
3.1. 海洋真核微生物冰核活性的多糖组分

In the Arctic marine environment, even during polar night, a sequencing-based survey of airborne marine eukaryotic microorganisms revealed an unexpected abundance of fungi (Figure S1). As a basis for the present study, we isolated and cultivated four different eukaryotic microorganisms present in the ocean and the atmosphere and studied their INA: (Figure 1) one thraustochytrid (T. striatum), two yeasts (T. pullulans, N. diffluens), and one filamentous fungus (P. chrysogenum). The marine microorganisms showed a significant spread of approximately 3 orders of magnitude at −15 °C. Compared to other INP types, these marine microbes induced freezing at higher temperatures than most types of desert dusts (above −18 °C) and at lower temperatures than (mainly proteinaceous) biogenic INMs from terrestrial origin (below −8 °C). Similar temperature dependencies among the different microorganisms indicated by a parametrization based on classical nucleation theory (CNT) (Figure 2) strongly suggest that the same chemical class of INMs is responsible for the observed INA, which was investigated in detail as described below:
在北极海洋环境中,即便在极夜期间,基于测序的空气中海洋真核微生物调查仍显示出真菌出人意料的丰度(图 S1)。作为本研究的基础,我们分离并培养了存在于海洋和大气中的四种不同真核微生物,并研究了它们的冰核活性(INA):(图 1)一种破囊壶菌(T. striatum)、两种酵母菌(T. pullulans, N. diffluens)和一种丝状真菌(P. chrysogenum)。这些海洋微生物在-15°C 时表现出约 3 个数量级的显著分布范围。与其他类型的冰核颗粒(INP)相比,这些海洋微生物诱发冻结的温度高于大多数沙漠尘埃类型(高于-18°C),而低于陆源(主要为蛋白质类)生物源冰核材料(INMs)(低于-8°C)。基于经典成核理论(CNT)的参数化分析表明(图 2),不同微生物间相似的温度依赖性强烈提示:观察到的冰核活性由同一化学类别的 INMs 所导致,具体研究如下:
(i)

To determine the molecular identity of the INMs, various physical and chemical tests were conducted on the microbial cultures. Filtration through a 0.2 μm filter reduced INM concentrations by 97–99.8% (Figure 2C), though still above background levels. This indicates that INMs are predominantly attached to microbial cells or aggregates, with a smaller portion existing as dissolved or colloidal substances. Heating the suspensions (95 °C for 1 h, Figure 2B,D) did not alter INM concentrations, suggesting a nonproteinaceous nature, as proteins typically lose their ice-nucleating activity at high temperatures. (46,66,83) In contrast, strong acid hydrolysis of the T. pullulans sample (0.05 M H2SO4, 100 °C, 72 h, Figure S2B) significantly reduced the ice fraction, implying that hydrolyzable macromolecules disintegrated into non-ice-active fragments. Together with the heat resistance, this points to the presence of ice-active polysaccharides, either free or bound to the surface of microorganisms or debris. Adding calcium chloride (1.6 g L–1) to the 0.2 μm filtered T. pullulans aliquot did not change the ice fraction, but subsequent filtration led to a substantial reduction (Figure S2E). This suggests that INMs in the dissolved fraction may be acidic polysaccharides, as they tend to form microgels with a cross-linked structure in the presence of divalent Ca2+ cations, resulting in particle sizes greater than 0.2 μm. (84,85) We hypothesize that particulate INMs, though not explicitly investigated here, may readily exist as such three-dimensional networks. Similarly, a standard solution of alginic acid, a commercially available acidic marine polysaccharide with the highest INA among those tested (Figure S2F), showed comparable behavior to the microorganism culture aliquots. As other cultures did not provide enough material only T. pullulans was characterized in more detail. Given the consistency of results across the different microbial cultures regarding physical treatments (Figure 2), we assume that these observations allow for a certain level of generalization.
为确定冰核物质(INMs)的分子特性,研究人员对微生物培养物进行了多项理化测试。0.2 μm 滤膜过滤使 INMs 浓度降低了 97-99.8%(图 2C),但仍高于背景水平,这表明 INMs 主要附着于微生物细胞或聚集体上,少部分以溶解态或胶体形式存在。悬浮液加热处理(95℃持续 1 小时,图 2B、D)未改变 INMs 浓度,暗示其非蛋白质本质——因为蛋白质通常在高温下会丧失冰核活性(46,66,83)。与之形成对比的是,短梗霉属样品经强酸水解(0.05 M H2SO4,100℃处理 72 小时,图 S2B)后冰核活性显著降低,表明可水解大分子已解离为无冰核活性的片段。结合耐热特性,这些现象说明存在游离态或结合于微生物/碎屑表面的冰活性多糖。向 0.2 μm 过滤后的短梗霉样品中添加氯化钙(1.6 g/L)未改变冰核活性,但后续过滤处理导致活性大幅下降(图 S2E)。 这表明溶解组分中的冰核物质可能是酸性多糖,因为它们倾向于在二价钙离子(Ca2+)存在下形成具有交联结构的微凝胶,从而导致粒径大于 0.2 微米。(84,85) 我们推测,虽然本文未明确研究颗粒状冰核物质,但它们很可能以这种三维网络形式存在。类似地,褐藻酸(一种市售的酸性海洋多糖,在所有测试样品中具有最高的冰核活性(图 S2F))的标准溶液,其行为与微生物培养液等分试样表现出可比性。由于其他培养物未能提供足够材料,仅对出芽短梗霉(T. pullulans)进行了更详细的表征。鉴于不同微生物培养物在物理处理方面结果的一致性(图 2),我们认为这些观察结果具有一定程度的普适性。

(ii)

To investigate polysaccharidic INA, standard polysaccharides commonly found in both, the marine and terrestrial environment, including laminarin, λ-carrageenan, κ-carrageenan, alginic acid (long- and short-chained), agar, cellulose, xanthan gum, and a lipopolysaccharide from P. aeruginosa were examined in a manner similar to the microbial samples. INA was found for all selected polysaccharide solutions. However, the different polysaccharides revealed a broad variability in terms of INA (Figure S3). The most ice-active polysaccharides with regard to observed onset temperature and number of INMs per dry mass were long-chained alginic acid and agar. It is important to note that, in the case of alginic acid, the qualitative experiments conducted (same as described under (i)) align closely with the observed behavior of the microorganism culture aliquots. Furthermore, agar and alginic acid are both negatively charged polysaccharides with gelling properties. However, other negatively charged polysaccharides, such as λ-carrageenan and κ-carrageenan, and neutral polysaccharides (cellulose, laminarin, lipopolysaccharide) showed an up to several orders of magnitude lower number concentration of INMs per dry mass. Additionally, an influence of the molecular weight is indicated as long-chained alginic acid (molecular weight: 100–200 kDa, degree of polymerization: 500–1000) was more ice-active than short-chained alginic acid (molecular weight: 2–40 kDa, degree of polymerization: 60–200). In summary, the sequence of monosaccharides within the polysaccharidic structure and their molecular weight had an influence on the INA of polysaccharides, although these features are obviously not the only relevant factor determining the INA. The effect of the secondary and tertiary three-dimensional structure on the catalysis of the ice nucleation has not been clarified. Previous studies also found an influence of chain length (86) and particle size (87) of biopolymers on their INA. However, the exact structures or features causing ice nucleation activity of biopolymers in general and in particular for polysaccharides remains elusive and more detailed experiments are required in the future.
为探究多糖类冰核活性物质,研究采用与微生物样本相似的方法,对海陆环境中常见的标准多糖进行了检测,包括昆布多糖、λ-卡拉胶、κ-卡拉胶(长链与短链)藻酸、琼脂、纤维素、黄原胶以及铜绿假单胞菌脂多糖。所有测试多糖溶液均呈现冰核活性,但不同多糖的冰核活性存在显著差异(图 S3)。就观测到的冰核起始温度及单位干质量冰核位点数而言,长链藻酸与琼脂表现出最强的冰核活性。值得注意的是,藻酸的定性实验结果(同(i)项所述方法)与微生物培养液等分试样的观测行为高度吻合。此外,琼脂与藻酸均为具有凝胶特性的带负电多糖。 然而,其他带负电的多糖(如λ-卡拉胶和κ-卡拉胶)以及中性多糖(纤维素、昆布多糖、脂多糖)每单位干质量所含冰核物质数量浓度要低几个数量级。此外,分子量的影响也得到体现——长链海藻酸(分子量:100-200 kDa,聚合度:500-1000)比短链海藻酸(分子量:2-40 kDa,聚合度:60-200)具有更强的冰活性。总体而言,多糖结构中单糖的排列顺序及其分子量会影响其冰核活性,但这些特征显然并非决定冰核活性的唯一相关因素。多糖二级和三级三维结构对冰核催化作用的影响尚未明确。先前研究还发现生物聚合物的链长(86)和粒径(87)对其冰核活性存在影响。 然而,导致生物大分子(尤其是多糖类物质)具有冰核活性的确切结构或特征仍不明确,未来需要开展更精细的实验研究。

(iii)

Polysaccharides in the cultivated microbial samples were detected in the dissolved and particulate phases, here referred to as total combined carbohydrates (TCCHO) (Table S3). The monosaccharide composition (Figure S4) revealed a complex mix of carbohydrates in all microorganisms contributing 4–66% to the total organic carbon. In the cultures of T. pullulans, T. striatum, and N. diffluens, the highest fraction of TCCHO was rather found in the particulate phase (76–91%) than in the dissolved phase (9–24%), which fits well to the strong reduction of INA after the filtration of these samples. Based on the monosaccharide footprint, strong indications for the presence of agar or agar-like ice-active polysaccharides within the microorganisms were found, while the presence of alginic acid could be excluded by the lack of mannuronic acid, a monosaccharide unit released during the acidic hydrolysis of alginic acid. The normalization of the INM number site density (eq S1) of the different microorganisms on a specific chemical measure─the carbohydrate carbon mass C-TCCHO─revealed a significant decrease of its spread between the different microbial samples from three to one order of magnitude (Figure 3, Figure 2A), which strongly indicates a causal relationship between C-TCCHO and INA. Additionally, a very high agreement of the INA of eukaryotic microorganisms and those of the marine polysaccharides alginic acid and agar could be found from the almost identical INM number site density normalized to C-TCCHO (Figure 3). As a result, we used INM number density normalized to C-TCCHO to parametrize INP resulting from polysaccharidic INMs in the marine organic aerosol (parametrization hereafter called HSZ25).
在培养的微生物样本中,多糖类物质以溶解态和颗粒态形式存在(统称为总结合碳水化合物 TCCHO,见表 S3)。单糖组成分析(图 S4)显示所有微生物样本中的碳水化合物均为复杂混合物,占总有机碳含量的 4%-66%。在出芽短梗霉、条纹特拉霉和流散诺卡氏菌的培养物中,TCCHO 主要存在于颗粒相(76%-91%),而非溶解相(9%-24%),这与样品过滤后冰核活性显著降低的现象高度吻合。根据单糖特征谱分析,研究发现了微生物体内存在琼脂或类琼脂冰活性多糖的强有力证据,而通过检测不到藻朊酸水解产物甘露糖醛酸,排除了藻朊酸存在的可能性。 将不同微生物的冰核位点密度(公式 S1)归一化至特定化学指标——碳水化合物碳质量 C-TCCHO 后,其在不同微生物样本间的离散度从三个数量级显著降低至一个数量级(图 3,图 2A),这强烈表明 C-TCCHO 与冰核活性(INA)存在因果关系。此外,通过 C-TCCHO 归一化后几乎完全一致的冰核位点密度值可见,真核微生物的冰核活性与海洋多糖(藻酸和琼脂)表现出高度一致性(图 3)。因此,我们采用 C-TCCHO 归一化的冰核位点密度参数化海洋有机气溶胶中多糖类冰核物质形成的冰核颗粒(该参数化方法下文称为 HSZ25)。

Figure 1  图 1

Figure 1. Ice nucleation site density per mass nm is given as a function of temperature for known mineral dust, biogenic INMs, and in this study examined marine microbial INMs. ‡This data was converted from ns or nv to nm. Details of the conversion are given in the SI. * The desert dust compilation includes Asian dust, Canary Island dust, Israeli dust, and Saharan dust. Refs (21,38−40,50,61,62,70,74−82)
图 1. 以单位质量 nm 计的冰核位点密度随温度变化的关系图,展示了已知矿物粉尘、生物源冰核物质(INMs)及本研究检测的海洋微生物源 INMs 的数据。‡该数据由 ns 或 nv 换算为 nm,具体换算方法见支持信息。*沙漠粉尘数据合集包含亚洲粉尘、加那利群岛粉尘、以色列粉尘和撒哈拉粉尘。参考文献(21,38−40,50,61,62,70,74−82)

Figure 2  图 2

Figure 2. Physical properties of analyzed eukaryotic microorganisms indicate a non proteinaceous origin of INMs mainly attached to the microbial cells. The INM number concentration per sample volume is given for unmodified eukaryotic microorganisms together with CNT-based fits (A) and after physical treatments: heating at 95 °C for 1 h (B), filtration (<0.2 μm; C) and the combination of both (D). Heating does not change INM number concentrations, whereas filtration significantly reduces INM number concentration, and subsequent heating does not alter the INM concentration. This points toward the existence of heat-stable most likely non proteinaceous INMs freely suspended and to a larger extent connected to microbial cells.
图 2. 真核微生物的物理特性分析表明,冰核物质(INMs)主要附着于微生物细胞且具有非蛋白质属性。图中展示了未经处理的真核微生物样本单位体积内 INM 数量浓度与基于碳纳米管(CNT)拟合曲线的对比(A),以及经物理处理后的数据:95℃加热 1 小时(B)、0.2μm 过滤(C)及两种处理的组合(D)。加热处理未改变 INM 浓度,而过滤显著降低 INM 数量浓度,后续加热处理亦未改变 INM 浓度。这表明存在热稳定的 INMs,这些物质很可能为非蛋白质结构,部分自由悬浮但更大比例与微生物细胞相关联。

In summary, the chemical identity of the INMs produced by the investigated marine eukaryotic microorganisms consists of polysaccharides either in their free form or bound to the microbial cell or fragments thereof. As described above, three arguments substantiate this conclusion: (i) targeted qualitative physical and chemical experiments elucidate a polysaccharidic nature of the INMs in the analyzed microbial samples, (ii) standard polysaccharides, which are also found in the marine and terrestrial environment, showed INA and behaved similarly compared to microbial samples, and (iii) TCCHO could be quantified (see the Experimental Methods section) and linked to observed INA. The spread of INM concentration of the various microbial samples reduces to less than 2 orders of magnitude (compare Figures 2A and 3). The similarity between the INA of microbial and standard polysaccharide samples and reduced spread, when normalized to C-TCCHO, strongly suggests polysaccharidic INMs as the cause of the observed freezing behavior in the microbial samples. Furthermore, with the conducted experiments we can rule out other potential macromolecular candidates, such as proteins, for inducing the observed ice formation (Figure 2). As a further conclusion, since marine INA polysaccharides (including alginic acid and agar) are also produced by other marine organisms, including globally distributed macro- and microalgae, (88−91) their importance is much greater on a global scale. Since several INA polysaccharides analyzed in this study show similar freezing behavior when normalized to C-TCCHO (Figure 3) and have a variety of biological sources, it is justified to consider the INA polysaccharides directly rather than the individual microorganisms to assess their global significance. The investigation of these biological sources, their emissions, vertical transport, and oceanic and atmospheric concentration of INA polysaccharides in detail is an interesting subject of future research. Finally, since we found different ice-active polysaccharides, which entails a certain diversity that is also reflected in the spread of nm, C-TCCHO in Figure 3, the individual curves of nm, C-TCCHO for each eukaryotic microorganism and marine polysaccharides are parametrized with the CNT-based model (the method is described in Section S6 SI, and the results are given in Table S4). In the following, we use the derived parametrization of T. striatum and declare it as HSZ25.
综上所述,所研究的海洋真核微生物产生的冰核活性物质(INMs)的化学本质是由游离态或与微生物细胞及其碎片结合的多糖构成。如前所述,三个论据支撑这一结论:(i)针对性定性物理化学实验阐明了所分析微生物样本中 INMs 的多糖特性;(ii)在海洋和陆地环境中同样存在的标准多糖表现出冰核活性(INA),其行为与微生物样本相似;(iii)总可溶性碳水化合物(TCCHO)可被定量检测(参见实验方法部分)并与观测到的 INA 相关联。不同微生物样本的 INM 浓度差异缩小至不足 2 个数量级(对比图 2A 与图 3)。当以 C-TCCHO 标准化后,微生物样本与标准多糖样本的 INA 相似性及差异缩小现象,强烈表明多糖类 INMs 是导致微生物样本中观测到结冰行为的原因。 此外,通过已开展的实验,我们可以排除其他潜在大分子物质(如蛋白质)引发观测到冰晶形成的可能性(图 2)。进一步结论表明,由于海洋冰核活性多糖(包括褐藻酸和琼脂)也由其他海洋生物产生,包括全球分布的宏藻与微藻,(88−91) 其在全球尺度上的重要性更为显著。鉴于本研究中分析的多种冰核活性多糖在归一化至 C-TCCHO 后呈现相似的冻结特性(图 3),且具有多样化的生物来源,直接评估冰核活性多糖而非单一微生物的全球影响是合理的。详细研究这些生物来源、其排放过程、垂直传输以及海洋与大气中冰核活性多糖的浓度,将成为未来研究中极具价值的课题。 最后,由于我们发现了多种具有冰活性的多糖,这种多样性也体现在图 3 中 nm,C-TCCHO 的分布上,因此我们采用基于经典成核理论(CNT)的模型对每种真核微生物和海洋多糖的 nm,C-TCCHO 单独曲线进行了参数化(方法详见 SI 第 S6 节,结果列于表 S4)。下文将采用条纹特拉伯菌(T. striatum)的推导参数化结果,并将其命名为 HSZ25。

Figure 3  图 3

Figure 3. High agreement of the ice nucleation activity of tested aquatic eukaryotic microorganisms with that of marine polysaccharides. The temperature-dependent ice nucleation site densities per carbohydrate carbon mass nm, C-TCCHO is presented with CNT-based parametrizations (parameters are presented in Table S4 in the SI). The derived CNT-parametrization of T. striatum is used for HSZ25.
图 3. 测试的水生真核微生物与海洋多糖的冰核活性高度吻合。图中展示了基于碳水化合物碳质量的温度依赖性冰核位点密度 nm,C-TCCHO,并采用基于经典成核理论(CNT)的参数化方法(相关参数见支持信息表 S4)。将 T. striatum 的 CNT 参数化结果应用于 HSZ25 样品。

3.2. Marine Polysaccharides Are Relevant Contributors to the INP Population in Remote Marine Regions Worldwide
3.2. 海洋多糖是全球偏远海域冰核颗粒群体的重要贡献组分

The importance of marine polysaccharidic INMs is estimated by applying the HSZ25 parametrization to marine polysaccharide concentrations derived from simulated sea salt mass and measured polysaccharide fractions in sea spray aerosol (0.5% in accumulation mode and 0.1% in coarse mode, see Sect. 2.3), in addition to INPs contributed by mineral dust. (70) The resulting INP concentrations were compared to worldwide available observations in the marine atmosphere (−20 to −15 °C: Figure 4 and Table S5, all observed temperatures: Figure S5). Note that by using only mineral dust and marine polysaccharides as INP types, the model is expected to underestimate the observed INP concentrations for temperatures >−15 °C (Figure S5). For such high temperatures, other INP types (e.g., proteinaceous INMs (92)) may account for the majority of INPs, which cannot be determined from the present study. Furthermore, terrestrial INPs other than mineral dust (e.g., terrestrial biological INPs) might contribute, as well.
通过将 HSZ25 参数化方法应用于海洋多糖浓度(该浓度源自模拟海盐质量及实测海喷雾气溶胶中的多糖占比:积聚模态 0.5%、粗模态 0.1%,详见第 2.3 节),并结合矿物尘埃贡献的冰核颗粒(INPs),评估了海洋多糖类冰核物质(INMs)的重要性。(70) 将计算得出的 INP 浓度与全球海洋大气观测数据(-20 至-15°C:图 4 和表 S5;全温度范围:图 S5)进行对比。需注意的是,由于模型仅考虑矿物尘埃和海洋多糖作为 INP 类型,预计会低估温度高于-15°C 时的观测 INP 浓度(图 S5)。在此高温区间,其他类型 INP(如蛋白质类冰核物质(92))可能占据主导地位,但本研究无法确定其具体贡献。此外,矿物尘埃以外的陆地 INP(如陆地生物源 INP)也可能产生一定影响。

Figure 4  图 4

Figure 4. Modeled against observed INP concentration between −15 and −20 °C. Measurement data from 14 different campaigns (n = 5364; see Tab S5 and Figure S6 for references and regional coverage) in predominantly marine air masses was used. These were compared to annual mean INP concentrations derived from modeled mineral dust and sea salt concentrations simulated with a global model. For mineral dust INPs, the parametrization by Niedermeier et al., (70) and for marine polysaccharide INPs, the parametrization derived in this work was applied. Gray dots show the comparison between modeled mineral dust INPs and observation, whereas colored dots (color-code by observation temperature) present the sum of modeled mineral dust + marine polysaccharide INPs. For orientation, the figure shows the 1:1 line (solid) and the 1:10 and 10:1 lines (dashed).
图 4. 在-15 至-20°C 温度范围内模拟与观测的冰核颗粒(INP)浓度对比。研究采用了来自 14 个不同观测活动(n=5364;具体参考文献及区域覆盖范围参见表 S5 和图 S6)的测量数据,这些数据主要来自海洋气团。将全球模式模拟的矿物沙尘与海盐浓度推算出的年平均 INP 浓度与观测值进行对比:矿物沙尘 INP 采用 Niedermeier 等人(70)的参数化方案,海洋多糖 INP 则采用本研究推导的参数化方案。灰色圆点表示模拟矿物沙尘 INP 与观测值的对比,而彩色圆点(按观测温度进行颜色编码)表示模拟矿物沙尘+海洋多糖 INP 的总和。图中标有 1:1 比例线(实线)及 1:10 和 10:1 比例线(虚线)作为参照基准。

Remarkably, despite its low concentration in remote marine regions mineral dust still provides a noticeable ubiquitous contribution to INPs at T < −15 °C even on the Southern Hemisphere consistent with previous model studies. (4,55,56) Considering the INMs from marine polysaccharides in addition to mineral dust INPs, the modeled total INP concentrations increased substantially for T > −20 °C, leading to a better agreement with the observations (Figure 4, Table S5). In the temperature range of −15 to −20 °C, the fraction of modeled INP concentrations that are within a factor of 2 and a factor of 10 to the observations, increases from 10 and 37% (when only accounting for mineral dust INPs), to 15 and 60%, respectively, for all Southern Ocean campaigns (Table S5). For individual campaigns, particularly in the remote Southern Ocean, even better agreement was found. Due to the higher abundance of mineral dust in the Northern Hemisphere, the relative contribution of nondust INPs is lower and the average simulation improvement is weaker for all considered INP data sets (agreement within a factor of 10 increasing from 52 to 63%). Variation of the polysaccharide content in the modeled sea spray aerosol in both modes to 0.05 and 0.5%, respectively, as lower and upper estimates, leads to an agreement within a factor of 10 of 47 and 86% for the Southern Ocean campaigns and of 56 and 77% for all campaigns (Table S5).
值得注意的是,尽管矿物粉尘在偏远海洋区域浓度较低,但在南半球温度低于-15°C 时仍对冰核粒子(INPs)具有显著且普遍存在的贡献,这与先前模型研究结果一致(4,55,56)。当在矿物粉尘 INPs 基础上加入海洋多糖来源的冰核物质(INMs)后,模型模拟的 INP 总浓度在温度高于-20°C 时显著增加,与观测数据吻合度明显提升(图 4,表 S5)。在-15 至-20°C 温度区间内,模拟 INP 浓度与观测值的偏差在 2 倍和 10 倍范围内的比例,对于所有南大洋航次而言,分别从 10%和 37%(仅考虑矿物粉尘 INPs 时)提升至 15%和 60%(表 S5)。个别航次(特别是偏远南大洋区域)的吻合度更为理想。由于北半球矿物粉尘丰度较高,非粉尘 INPs 的相对贡献较低,所有 INP 数据集的平均模拟改进幅度较弱(10 倍偏差范围内的吻合比例从 52%提升至 63%)。 将模拟海盐气溶胶中两种模态的多糖含量分别调整为 0.05%和 0.5%作为下限和上限估计值时,南大洋航次观测数据的吻合度达到 47%至 86%(相差 10 倍以内),所有航次数据的吻合度为 56%至 77%(表 S5)。
The concentration of marine INPs in sea spray aerosol can be represented by a previously developed parametrization that uses sea spray aerosol surface area as proxy (59) (hereafter M18). However, M18 was developed based on samples that were not heat-labile, indicating only minor contributions from, e.g., proteinaceous compounds. By applying the M18 parametrization to the modeled sea salt concentration instead of HSZ25, a similar improvement (i.e., INPs in addition to mineral dust INPs) can be obtained, primarily with better agreement to observations (fraction in factor of 2 and factor of 10, see Table S5). To compare the performance of the two parametrizations, the increase in agreement within a factor of 10 (in addition to mineral dust only) is used (eq 1). Across the different Southern Ocean data sets and in the temperature range of −15 to −20 °C, the HSZ25 parametrization reproduces between ∼30 and 115% of this increased agreement within a factor of 10 found for the M18 parametrization (44% on average for all observational data sets including Northern Hemisphere). The reproduced fraction is still 10–100% in the Southern Ocean (19% for all campaigns) for a polysaccharide content of 0.05%, increasing toward the upper bounds of polysaccharide content of 0.5 to 100–120% in the Southern Ocean (104% for all campaigns) as shown in Table S5. Hence, polysaccharides, which are the only considered compound group in HSZ25, can explain a large fraction up to all marine INPs (as seen in M18) within −15 to −20 °C. The discrepancy between the two parametrizations might be caused by their general uncertainties (e.g., total marine INPs in SSA can include other compounds than the polysaccharides applied in this study), the assumed polysaccharide content and its spatiotemporal variability that is currently not covered by the applied model, and other INP types that might have been present in the samples that M18 is based on (e.g., more efficient INA polysaccharides).
海喷雾气溶胶中海洋冰核粒子(INPs)的浓度可采用先前开发的参数化方案表示,该方案以海喷雾气溶胶表面积作为代用指标(59)(下文简称 M18)。但 M18 是基于非热不稳定性样品建立的,表明其中蛋白质类化合物等成分贡献较小。将 M18 参数化方案应用于模拟海盐浓度(而非 HSZ25)时,可获得类似的改进效果(即在矿物尘 INPs 基础上新增的 INPs),主要表现为与观测数据更吻合(2 倍和 10 倍范围内的符合比例见表 S5)。为比较两种参数化方案的性能,采用 10 倍范围内(在仅含矿物尘基础上)的符合度提升作为评价指标(公式 1)。在南大洋不同数据集和-15 至-20°C 温度区间内,HSZ25 参数化方案对 M18 方案 10 倍范围内符合度提升量的再现率为 30%~115%(包含北半球的所有观测数据集平均为 44%)。 在南大洋(所有航次平均 19%),当多糖含量为 0.05%时,重现比例仍达 10-100%;如表 S5 所示,随着多糖含量升至 0.5%的上限,该比例在南大洋(所有航次平均 104%)增至 100-120%。因此,作为 HSZ25 中唯一考虑的化合物类别,多糖在-15 至-20°C 范围内可解释大部分乃至全部海洋冰核粒子(如 M18 所示)。两种参数化方案的差异可能源于:其普遍不确定性(例如海盐气溶胶中的总海洋冰核粒子可能包含本研究未涉及的其他化合物)、假设的多糖含量及其时空变异性(当前模型尚未涵盖)、以及 M18 样本中可能存在的其他冰核类型(如成冰活性更高的多糖)。
At the higher end of the relevant temperature range (−15 to −16 °C), on annual average, the INP concentrations resulting from marine polysaccharides are comparable to or exceed the INP concentrations from mineral dust in most parts of the marine atmosphere and in particular on the Southern Hemisphere (Figure 5). For a lower temperature, the importance of the INPs from marine polysaccharides decreases as mineral dust increases. Over the remote oceans of the Southern Hemisphere, the modeled INPs from marine polysaccharides are comparable to INPs from mineral dust down to about −19 °C and thus represent an important contributor to INPs in remote marine regions in a temperature range relevant for mixed-phase clouds. For lower temperatures, mineral dust INPs always dominate.
在相关温度范围的高端(-15 至-16°C),海洋多糖产生的冰核颗粒(INP)浓度在海洋大气大部分区域(尤其是南半球)的年平均值与矿物尘 INP 浓度相当或更高(图 5)。当温度较低时,海洋多糖 INP 的重要性随矿物尘 INP 的增加而降低。在南半球偏远海域,模型模拟显示海洋多糖 INP 在低至约-19°C 时仍与矿物尘 INP 浓度相当,因此在混合相云相关的温度范围内,海洋多糖是偏远海域 INP 的重要来源。当温度更低时,矿物尘 INP 始终占据主导地位。

Figure 5  图 5

Figure 5. Percentage of modeled polysaccharide-based marine INPs in the sum of modeled INPs (mineral dust + marine polysaccharides) in the lowermost model layer for different temperatures. Annual mean INP concentrations were derived from mineral dust concentrations and from polysaccharides estimated based on sea salt concentrations simulated by a global model.
图 5. 最底层模式中不同温度下模拟的基于多糖的海洋冰核粒子(INPs)占模拟 INPs 总量(矿物粉尘+海洋多糖)的百分比。年均 INP 浓度由矿物粉尘浓度和基于全球模式模拟的海盐浓度估算的多糖浓度得出。

3.3. Implications for Modeling of INPs
3.3 对冰核粒子建模的启示

In the present study, we show that in the temperature range from −15 to −20 °C, a significant part of the temperature-dependent INP number concentration in the marine atmosphere can be described based on a single relevant chemical component, ice-active marine polysaccharides. The CNT-based physical foundation of the chosen parametrization function has advantages for the application in atmospheric models as it reproduces observed INP-type-specific natural limits, i.e., realistic representation of freezing onset and implicitly comprising an upper limit of resulting INPs. Hence, possibly invalid extrapolation of log-linear parametrizations into temperature ranges that are not supported by measured data is avoided. Further, the concept is applicable to other INP sources and types, e.g., land-based biological INMs or specific ice-active mineral dust components, and allows for a time-dependent description of freezing using the nucleation rate (applying derived parameters of the contact angle distribution) instead of ice nucleation site density.
本研究表明,在-15 至-20°C 温度区间内,海洋大气中与温度相关的冰核数浓度主要部分可通过单一关键化学成分——具有冰活性的海洋多糖——进行描述。所选参数化函数基于经典成核理论(CNT)的物理基础,在大气模型应用中具有优势:它能复现观测到的冰核类型特异性自然极限,即真实呈现冻结起始温度并隐含最终冰核数量的上限。由此避免了传统对数线性参数化向无实测数据支持的温度区间进行可能无效的外推。此外,该模型框架可推广至其他冰核来源与类型(如陆源生物冰核物质或特定冰活性矿物粉尘组分),并能通过成核速率(应用接触角分布推导参数)而非冰核位点密度来实现冻结过程的时间依赖性描述。
As a perspective, the present study pilots a way toward enhanced process understanding of ice formation by describing the total INP concentration using a combination of ice-active chemical classes that are causally linked to ice formation instead of using proxy aerosol properties that are only correlated with INA. Although this concept requires research on ice-active chemical classes, their emission pathways, and their atmospheric distribution, it would enable atmospheric models to directly relate ice formation and cloud glaciation to the occurrence of the relevant causes with realistic spatiotemporal variability of INPs. Modeling approaches for emission of, e.g., mineralogy of mineral dust (93) and marine biological macromolecule classes do exist (94) allowing for such a causal description of the total INP concentration.
从研究视角来看,本研究通过采用与冰形成存在因果关联的冰活性化学物质类别(而非仅与冰核活性相关的替代性气溶胶特性)来描述总冰核颗粒浓度,为深化冰形成过程认知开辟了新路径。尽管该理念仍需对冰活性化学物质类别、其排放途径及大气分布开展研究,但将使大气模型能够将冰形成与云冰晶化过程直接关联到具有真实时空变异性的关键成因上。目前针对矿物粉尘矿物学特征(93)和海洋生物大分子类别排放的建模方法已然存在(94),这为总冰核颗粒浓度的因果性描述提供了实现基础。
The significant role of a natural biogenic aerosol constituent for the atmospheric INP budget highlights the importance of the coupling between biosphere and atmosphere in the Earth System. While anthropogenic aerosol emissions are expected to decrease with mitigation strategies to climate change, (95) natural aerosol particles will become even more important for cloud microphysics. Clouds in a cleaner environment, i.e., with a low droplet number (“aerosol limited regime”), are more sensitive to variability in aerosol number concentration. (96,97) Furthermore, it is important to note that mineral dust emissions were and are subject to regionally differing changes. (98−100) Overall, as anthropogenic sources do not contribute significantly to the atmospheric INP budget, (101,102) the number relation between cloud droplets and INPs might change in a less polluted atmosphere, with implications for cloud phase in mixed-phase clouds and therefore on cloud radiative forcing.
天然生物气溶胶组分对大气冰核粒子(INP)预算的重要作用,凸显了地球系统中生物圈与大气圈耦合的关键意义。随着气候变化减缓策略的实施,人为气溶胶排放预计将减少(95),自然气溶胶粒子对云微物理过程的影响将更为突出。在更清洁的环境中(即处于"气溶胶限制状态"的低云滴数条件下),云对气溶胶数浓度变化的敏感性会显著增强(96,97)。此外需特别注意,矿物沙尘排放始终存在区域差异性变化特征(98−100)。总体而言,由于人为源对大气 INP 预算贡献有限(101,102),在污染较轻的大气中,云滴与 INP 的数量关系可能发生改变,进而影响混合相云的云相态,最终作用于云辐射强迫效应。

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PolysaccharidesImportant Constituents of Ice-Nucleating Particles of Marine Origin

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Supporting Information for Publication
出版支持信息
Polysaccharides - Important Constituents of
多糖类——海洋源冰核粒子的重要组分
Ice Nucleating Particles of Marine Origin
海洋源冰核粒子
Susan Hartmann,  苏珊·哈特曼,
,
,
Roland Schrödner,  罗兰·施罗德纳,
,
,
Brandon T. Hassett,  布兰登·T·哈塞特,
§
Markus  马库斯
Hartmann,  哈特曼
Manuela van Pinxteren,  曼努埃拉·范·平克斯特伦
Khanneh Wadinga Fomba,  卡内·瓦丁加·丰巴
Frank  弗兰克
Stratmann,
Hartmut Herrmann,
Mira Pöhlker,
and Sebastian Zeppenfeld
,
Department of Atmospheric Microphysics (AMP), Leibniz Institute for Tropospheric
Research (TROPOS), Leipzig, 04318, Germany.
These authors contributed equally to this work.
Department of Modeling Atmospheric Processes (MOD), Leibniz Institute for
Tropospheric Research (TROPOS), Leipzig, 04318, Germany.
§
Department of Arctic and Marine Biology, UiT – The Arctic University of Norway,
Tromsø, 9019, Norway.
Atmospheric Chemistry Department (ACD), Leibniz Institute for Tropospheric Research
(TROPOS), Leipzig, 04318, Germany
E-mail: susan.hartmann@tropos.de; roland.schroedner@tropos.de
Summary: 26 pages, 7 figures, 5 tables.
S1
S1 Further explanations to Figure 1
Ice nucleation data is typically presented as nucleation site density per volume (
n
v
), surface
area (
n
s
), or mass (
n
m
). In order to visualize the data using the same metric, here we chose
n
m
, it necessary to convert reported
n
s
and
n
v
into
n
m
. For the conversion from
n
v
to
n
m
,
the total mass of material was required. Following Xi et al. (2021),
1
we estimated the total
mass by employing the number of cells reported in the respective publication, the cell volume
as given in the literature, and a assuming a cell density of 1 gcm
3
. If the literature directly
reported a cell volume, that volume was used. If the diameter along two perpendicular axes
was reported, the shape of the cell was assumed to be a prolate spheroid and the volume
calculated accordingly, and if only one cell diameter was reported, the cell shape was assumed
to be a sphere. For the microorganisms reported in Creamean et al. (2020)
2
the respective
values were taken from Kocur and Hodgkiss (1973),
3
Elshaded et al. (2004),
4
Sublimi et
al. (2011),
5
and Tindall et al. (1984).
6
For the species in Ickes et al. (2020)
7
the values
are taken from Olenina et al. (2006).
8
For the species in this study, the TOC mass was as
the closest available parameter to the total material mass. For the conversion from
n
s
to
n
m
of microbial INMs, a cell density of 1 g cm
3
was assumed as before. Information on the
shape and diameter of the cells was again taken from the literature, and the surface area
of the cells and thus their volume was calculated accordingly. For the species reported by
Haga et al. (2013, 2014),
9,10
Morris et al. (2013),
11
Jayweera and Flanagan (1982),
12
and
Iannone et al. (2011)
13
the
n
s
data was extracted from Haga et al. (2014)
9
and converted
with the geometric parameters therein. For the conversion from
n
s
to
n
m
of the mineral
dusts we assume spherical particles with a diameter of 662 nm and certain densities. This
diameter is the modal value of the particle volume size distribution (PVSD) of heavy dust
episodes in the 10-year long dataset of aerosol particle measurements at Cabo Verde by
Gong et al. (2022).
14
Since this represents the particle diameter that contributes most to
the particle mass in natural mineral dust, it is a reasonable simplification in lack of PVSDs
for the mineral dusts used in the cited studies. As the bulk density of mineral dust we used
S2

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Author Information  作者信息

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  • Corresponding Authors  通讯作者
    • Susan Hartmann - Department of Atmospheric Microphysics (AMP), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, GermanyOrcidhttps://orcid.org/0000-0002-9556-2772 Email: susan.hartmann@tropos.de
      苏珊·哈特曼 - 德国莱比锡 04318,莱布尼茨对流层研究所(TROPOS)大气微物理系(AMP); Orcid https://orcid.org/0000-0002-9556-2772;电子邮箱:susan.hartmann@tropos.de
    • Roland Schrödner - Department of Modeling Atmospheric Processes (MOD), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, GermanyOrcidhttps://orcid.org/0000-0003-1185-6018 Email: roland.schroedner@tropos.de
      罗兰·施罗德纳 - 德国莱比锡 04318,莱布尼茨对流层研究所(TROPOS)大气过程模拟系(MOD); Orcid https://orcid.org/0000-0003-1185-6018;电子邮箱:roland.schroedner@tropos.de
  • Authors  作者
    • Brandon T. Hassett - Department of Arctic and Marine Biology, UiT − The Arctic University of Norway, Tromsø 9019, NorwayOrcidhttps://orcid.org/0000-0002-1715-3770
      布兰登·T·哈塞特 - 挪威北极大学北极与海洋生物系,挪威特罗姆瑟 9019; Orcid https://orcid.org/0000-0002-1715-3770
    • Markus Hartmann - Department of Atmospheric Microphysics (AMP), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, GermanyOrcidhttps://orcid.org/0000-0001-9700-1701
      马库斯·哈特曼 - 对流层研究所大气微物理系(AMP),德国莱比锡 04318; Orcid https://orcid.org/0000-0001-9700-1701
    • Manuela van Pinxteren - Atmospheric Chemistry Department (ACD), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, GermanyOrcidhttps://orcid.org/0000-0002-8746-8620
      曼努埃拉·范·平克斯特伦 - 对流层研究所大气化学系(ACD),德国莱比锡 04318; Orcid https://orcid.org/0000-0002-8746-8620
    • Khanneh Wadinga Fomba - Atmospheric Chemistry Department (ACD), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, GermanyOrcidhttps://orcid.org/0000-0002-4952-4863
      Khanneh Wadinga Fomba - 德国莱比锡 04318,对流层研究所(TROPOS)大气化学部(ACD); Orcid https://orcid.org/0000-0002-4952-4863
    • Frank Stratmann - Department of Atmospheric Microphysics (AMP), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, GermanyOrcidhttps://orcid.org/0000-0003-1977-1158
      Frank Stratmann - 德国莱比锡 04318,对流层研究所(TROPOS)大气微物理部(AMP); Orcid https://orcid.org/0000-0003-1977-1158
    • Hartmut Herrmann - Atmospheric Chemistry Department (ACD), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, GermanyOrcidhttps://orcid.org/0000-0001-7044-2101
      哈特穆特·赫尔曼 - 德国莱比锡 04318,莱布尼茨对流层研究所大气化学部; Orcid https://orcid.org/0000-0001-7044-2101
    • Mira Pöhlker - Department of Atmospheric Microphysics (AMP), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, Germany
      米拉·珀尔克 - 德国莱比锡 04318,对流层研究所(TROPOS)大气微物理系(AMP)
    • Sebastian Zeppenfeld - Atmospheric Chemistry Department (ACD), Leibniz Institute for Tropospheric Research (TROPOS), Leipzig 04318, GermanyOrcidhttps://orcid.org/0000-0003-4622-3181
      Sebastian Zeppenfeld - 德国莱比锡 04318,对流层研究所(TROPOS)大气化学部(ACD); Orcid https://orcid.org/0000-0003-4622-3181
  • Author Contributions  作者贡献

    S.H., R.S., and S.Z. contributed equally to this work.
    S.H.、R.S.和 S.Z.对本工作贡献均等。

  • Notes  注释
    The authors declare no competing financial interest.
    作者声明无竞争性经济利益。

Acknowledgments  致谢

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We thank Anke Rödger, Amelie Assenbaum, and Josephine Gundlach for the OC/EC and INP measurements, respectively. We are grateful to Paul DeMott, his colleagues, and André Welti for sharing their comprehensive data sets and Dennis Niedermeier for providing CNT-based dust parametrization. Funding for the research is provided by Leibniz Institute for Tropospheric Research (TROPOS) internal funding (R.S., S.H., S.Z.) and Deutsche Forschungsgemeinschaft (DFG, German Research Foundation, Projektnummer 268020496-TRR 172) within the Transregional Collaborative Research Center ArctiC Amplification: Climate Relevant Atmospheric and SurfaCe Processes, and Feedback Mechanisms (AC)3 in subproject B04 (S.Z., F.S., and M.v.P.).
我们分别感谢 Anke Rödger、Amelie Assenbaum 和 Josephine Gundlach 进行的有机碳/元素碳(OC/EC)和冰核颗粒(INP)测量。衷心感谢 Paul DeMott 及其同事,以及 André Welti 分享其综合数据集,同时感谢 Dennis Niedermeier 提供基于经典成核理论(CNT)的沙尘参数化方案。本研究经费由莱布尼茨对流层研究所(TROPOS)内部资金(R.S.、S.H.、S.Z.)和德国研究基金会(DFG,项目编号 268020496-TRR 172)通过跨区域合作研究中心"北极放大:气候相关大气与地表过程及反馈机制(AC)³"的 B04 子项目(S.Z.、F.S.和 M.v.P.)提供。

References  参考文献

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  • Abstract  摘要

    Figure 1  图 1

    Figure 1. Ice nucleation site density per mass nm is given as a function of temperature for known mineral dust, biogenic INMs, and in this study examined marine microbial INMs. ‡This data was converted from ns or nv to nm. Details of the conversion are given in the SI. * The desert dust compilation includes Asian dust, Canary Island dust, Israeli dust, and Saharan dust. Refs (21,38−40,50,61,62,70,74−82)
    图 1. 以单位质量 nm 计的冰核位点密度随温度变化的关系图,展示了已知矿物粉尘、生物源冰核物质(INMs)及本研究检测的海洋微生物源 INMs 的数据。‡该数据由 ns 或 nv 换算为 nm,具体换算方法见支持信息。*沙漠粉尘数据合集包含亚洲粉尘、加那利群岛粉尘、以色列粉尘和撒哈拉粉尘。参考文献(21,38−40,50,61,62,70,74−82)

    Figure 2  图 2

    Figure 2. Physical properties of analyzed eukaryotic microorganisms indicate a non proteinaceous origin of INMs mainly attached to the microbial cells. The INM number concentration per sample volume is given for unmodified eukaryotic microorganisms together with CNT-based fits (A) and after physical treatments: heating at 95 °C for 1 h (B), filtration (<0.2 μm; C) and the combination of both (D). Heating does not change INM number concentrations, whereas filtration significantly reduces INM number concentration, and subsequent heating does not alter the INM concentration. This points toward the existence of heat-stable most likely non proteinaceous INMs freely suspended and to a larger extent connected to microbial cells.
    图 2. 真核微生物的物理特性分析表明,冰核物质(INMs)主要附着于微生物细胞且具有非蛋白质属性。图中展示了未经处理的真核微生物样本单位体积内 INM 数量浓度与基于碳纳米管(CNT)拟合曲线的对比(A),以及经物理处理后的数据:95℃加热 1 小时(B)、0.2μm 过滤(C)及两种处理的组合(D)。加热处理未改变 INM 浓度,而过滤显著降低 INM 数量浓度,后续加热处理亦未改变 INM 浓度。这表明存在热稳定的 INMs,这些物质很可能为非蛋白质结构,部分自由悬浮但更大比例与微生物细胞相关联。

    Figure 3  图 3

    Figure 3. High agreement of the ice nucleation activity of tested aquatic eukaryotic microorganisms with that of marine polysaccharides. The temperature-dependent ice nucleation site densities per carbohydrate carbon mass nm, C-TCCHO is presented with CNT-based parametrizations (parameters are presented in Table S4 in the SI). The derived CNT-parametrization of T. striatum is used for HSZ25.
    图 3. 测试的水生真核微生物冰核活性与海洋多糖高度吻合。基于碳水化合物碳质量的温度依赖性冰核位点密度 nm,C-TCCHO 采用经典成核理论(CNT)参数化呈现(参数见 SI 表 S4)。条纹颤藻(T. striatum)的 CNT 参数化结果被用于 HSZ25 样品分析。

    Figure 4  图 4

    Figure 4. Modeled against observed INP concentration between −15 and −20 °C. Measurement data from 14 different campaigns (n = 5364; see Tab S5 and Figure S6 for references and regional coverage) in predominantly marine air masses was used. These were compared to annual mean INP concentrations derived from modeled mineral dust and sea salt concentrations simulated with a global model. For mineral dust INPs, the parametrization by Niedermeier et al., (70) and for marine polysaccharide INPs, the parametrization derived in this work was applied. Gray dots show the comparison between modeled mineral dust INPs and observation, whereas colored dots (color-code by observation temperature) present the sum of modeled mineral dust + marine polysaccharide INPs. For orientation, the figure shows the 1:1 line (solid) and the 1:10 and 10:1 lines (dashed).
    图 4. 在-15 至-20°C 温度范围内模拟与观测的冰核颗粒(INP)浓度对比。研究采用了来自 14 个不同观测活动(n=5364;具体参考文献及区域覆盖范围参见表 S5 和图 S6)的测量数据,这些数据主要来自海洋气团。将全球模式模拟的矿物沙尘与海盐浓度推算出的年平均 INP 浓度与观测值进行对比:矿物沙尘 INP 采用 Niedermeier 等人(70)的参数化方案,海洋多糖 INP 则采用本研究推导的参数化方案。灰色圆点表示模拟矿物沙尘 INP 与观测值的对比,而彩色圆点(按观测温度进行颜色编码)表示模拟矿物沙尘+海洋多糖 INP 的总和。图中标有 1:1 比例线(实线)及 1:10 和 10:1 比例线(虚线)作为参照基准。

    Figure 5  图 5

    Figure 5. Percentage of modeled polysaccharide-based marine INPs in the sum of modeled INPs (mineral dust + marine polysaccharides) in the lowermost model layer for different temperatures. Annual mean INP concentrations were derived from mineral dust concentrations and from polysaccharides estimated based on sea salt concentrations simulated by a global model.
    图 5. 最底层模式中不同温度下模拟的基于多糖的海洋冰核粒子(INPs)占模拟 INPs 总量(矿物粉尘+海洋多糖)的百分比。年均 INP 浓度由矿物粉尘浓度和基于全球模式模拟的海盐浓度估算的多糖浓度得出。

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