2022, Vol. 62中国科学院微生物研究所，中国微生物学会
文章信息
- 雷婷婷, 陈良仲, 陈绍兴, 沈亮. 2022
- LEI Tingting, CHEN Liangzhong, CHEN Shaoxing, SHEN Liang.
- 微生物对低温极端环境适应性的研究进展
- Progress in research on the adaptability of microorganisms to extremely cold environments
- 微生物学报, 62(6): 2150-2164
- Acta Microbiologica Sinica, 62(6): 2150-2164
-
文章历史
- 收稿日期：2021-10-24
- 修回日期：2022-01-15
- 网络出版日期：2022-03-16
引用本文 |
2. 安徽师范大学生态与环境学院，安徽 芜湖 241002
2. School of Ecology and Environment, Anhui Normal University, Wuhu 241002, Anhui, China
温度常年低于5 ℃的环境一般被认为是永久寒冷环境，地球上75%的生物圈处于永久寒冷环境中(南极、北极、高山地区、深海、冰洞和大气层上层等)[1]。被大型地理屏障所隔离的南极、北极以及青藏高原冰川和冻土环境的温度常年低于0 ℃，是地球上的极端寒冷环境。本文主要总结关于极端寒冷环境微生物适应性的研究进展[2-4]。通过与全球尺度微生物群落组成对比，可发现在大的分类单元上，极端寒冷环境中的微生物群落与其他环境存在一些明显差别[5-6]。如在冰川环境中以β-变形菌纲(Betaproteobacteria)为主，在海冰中以黄杆菌纲(Flavobacteriia)和γ-变形菌纲(Gammaproteobacteria)为主，在冻土以放线菌门(Actinobacteria)为主[5]。从低温代谢(尤其是温度低于0 ℃)能力的角度看，极地和山地高寒环境中微生物的活性显著高于其他非寒冷环境中的近缘物种[7-10]。嗜冷微生物(嗜冷菌的定义在下文中讨论)是驱动广阔寒冷环境中关键的生物地球化学循环的重要生物因素，并且对气候环境变化十分敏感[11-13]。例如，气候变暖可能会促进冰川微生物介导的有机碳转化，而形成微生物来源的有机碳释放增加-反照率下降-冰川消融加速等反馈机制[14]。
气候变暖还可能导致冰川环境特有的嗜冷微生物类群(specialist taxa)丧失竞争优势，而被广布类群(generalist taxa)或者中温类群替代[10, 15]。极端低温环境中的微生物不仅可以指示气候变化，其良好的低温活性也预示着嗜冷菌在工业节能减排和山地高寒农田增收中有着广阔的应用前景[16-17]。
1 最适和最高生长温度特征定义嗜冷菌的局限性嗜冷菌通常被定义为最适生长温度接近或者低于15 ℃，最高生长温度低于20 ℃，最低生长温度为0 ℃或者更低的微生物。在4 ℃或者以下能够生长，最高生长温度高于20 ℃则被认为是耐冷微生物[18-20]。但基于生长温度特征定义的嗜冷菌和耐冷菌的概念很难准确描述一个细菌适应寒冷环境的能力及其在寒冷环境中生态功能的强弱[9, 21]。因为当温度上升时，酶的活性通常也将上升，细菌的生长速率随之上升，一直到受某个温度的限制。因此，最高生长温度仅仅定义了微生物能耐受的最高温度，而不能衡量其低温适应能力。实际上大部分从寒冷环境分离的细菌都能够在高于它们分离环境的温度中生长良好。如一个嗜冷菌可以耐受30 ℃以上的生长温度，这株菌就应该被定义成嗜中温菌，这不符合实际情况[21]。基于这个逻辑，就出现了一个问题：这些含义不清晰的名词嗜冷菌、耐冷菌和兼性嗜冷菌为什么会被经常用到？自1967年Farrell和Rose提出嗜冷菌概念以来，微生物学家在如何准确定义和使用嗜冷菌这个问题上难以达成一致[21-22]。直到2016年Cavicchioli在已有的研究基础上通过对比分析，认为只要细菌能够在寒冷环境中自然生长并发挥生态功能，即可认为它们是适应寒冷环境的，并建议将这些能够适应寒冷环境的细菌统称为嗜冷菌[21-23]; 如这些嗜冷菌能够在系统发育树上形成(可操作)单系类群，则可称之为低温环境特有类群[10]。实际上，即使在-1 ℃或者0 ℃生长良好的细菌，仍然可在20 ℃以上的温度生长，但这并不意味着这类微生物不是嗜冷菌或者低温环境特有类群[8, 10, 24-25]。
到目前为止，微生物生长温度的下限还没有明确的概念，但有研究认为，微生物繁殖的温度下限为-12 ℃，维持细胞代谢的温度下限约为-40 ℃[7, 26]。嗜冷菌在低温(-8 ℃)的生长曲线往往不呈指数形，而是表现为线性或者是逐渐下降的曲线[27]。利用稳定同位素标记分析发现，在北极冻土中的微生物可在-16 ℃保持群落水平的代谢活性，涵盖了9个门，10个科。这项研究还发现Melioribacteriaceae、疣微菌科(Verrucomicrobiaceae)和Candidatus Saccharibacteria (TM7)中的一些分类单元与来自其他低温环境相似类群形成了可在零下保持活性的群簇[28]。低温对细胞会产生一系列的物理化学限制，如影响细胞完整性、水的粘滞性、溶质的融化速率、细胞膜流动性、酶活性和大分子之间的相互作用[29-30]。有证据表明，微生物在低温下(-40 ℃)有活性，那微生物必定会有相应的适应性策略来应对低温环境造成的不利影响。因此，嗜冷菌进化出了相应的机制从而使它们成功地在寒冷环境中存活[31-32]。围绕微生物如何适应寒冷环境，已开展了大量的研究，包括生理学和近些年发展起来的组学研究。通过组学和生理学相结合的方法，在微生物适应寒冷环境的机制方面取得了丰富的成果。
2 低温微生物的适应机制 2.1 基因组GC含量、RNA二级结构与低温适应性微生物(细菌和古菌)的基因组由环状或线性的双链DNA组成[33]，在双链DNA序列中，GC碱基对比AT碱基对之间多一个氢键，GC含量的改变被认为会影响DNA双链的稳定性，从而与微生物的生长温度相关[34]。但是在嗜冷、嗜热和中温菌之间，全基因组GC含量与最适生长温度之间缺乏统一的显著相关性[34-35]。不过最近有研究发现，最适生长温度较低的冷杆菌属(Cryobacterium)菌株，其基因组第三位密码子GC含量要低于同属最适生长温度较高的菌株[36]; 节细菌属(Arhtrobacter)的极地和山地环境嗜冷类群(polar and alpine psychrophilic lineage)全基因组GC含量要显著低于同属其他非极地环境的中温菌株[10]，这些显著相关性只局限在一些类群中，不具有普适性[35, 37]。虽然全基因组GC含量与最适生长温度之间缺乏普遍的相关性，但是在大部分微生物类群中，RNA的二级结构(rRNA茎环结构中的茎，tRNA的三叶草结构中的茎)与GC含量之间显著正相关，嗜冷微生物RNA的GC含量要低于中温菌和嗜热菌[38]。对于含有多拷贝16S rRNA基因的微生物，在较低的生长温度条件下，倾向于表达GC含量低的16S rRNA基因，这进一步支持了RNA的GC含量与生长温度密切相关[39]。
2.2 蛋白质氨基酸组成的调整以获得低温下活性恒温动物可在寒冷中保持合适的体温，其细胞内的代谢活动在一个大致恒定的温度中进行。而微生物与其环境则处于完全热平衡状态，嗜冷菌细胞的所有组成部分都必须适应低温，从整体上实现维持生长和生存的细胞功能[40]。作为生命的物质基础，蛋白质是生命活动的主要承担者。蛋白质如何保持低温下的活性，是微生物在低温环境下实现生长和发挥功能所要解决的首要问题[29, 41]。通过比较基因组学和蛋白质结构分析的方法研究发现，改变特定氨基酸的比例可改变蛋白质的热稳定性和底物亲和力，从而维持低温下的活性。如降低精氨酸(arginine)和脯氨酸(proline)含量，可减少氢键和盐桥，增强蛋白质构象的柔性，提高酶在低温下的活性; 相应地，赖氨酸(lysine)、异亮氨酸(isoleucine)和谷氨酰胺(glutamine)的含量会增加。从氨基酸性质上看，整体表现为极性氨基酸比例的增加，酸性氨基酸比例的减少，而疏水性氨基酸在不同蛋白质中的变化趋势并不完全一致[42]。用精氨酸代替赖氨酸使得嗜冷α-淀粉酶构象更稳定、活性更低，表现出嗜中温酶的特征，这为赖氨酸残基在促进酶冷适应中的重要性提供了实验支持[43]。上述趋势也在嗜冷酶[白三烯A4水解酶，leukotriene A4 hydrolase; C β-内酰胺酶，C β-lactamase]中得到了验证[44-45]。通过增加带有疏水侧链氨基酸在溶质接触区域的含量，减少疏水残基在酶核心区域的含量来提高低温下酶的催化效率则在嗜冷白三烯A4水解酶中得到了验证[44]。增长外部环状结构的长度，减少脯氨酸的含量从而降低蛋白质稳定性，可增加嗜冷蛋白质的折叠活性和运动性，此现象在嗜冷酶[异三烯A4水解酶(alleuotriene A4 hydrolasehe)和纤维素酶(cellulase)]上也得到了验证[46-47]。上述蛋白质序列和构象的改变，可使底物更容易接近酶的活性中心，从而降低活化能，保证微生物在低温下足够的代谢活性[48-49]。高分辨率的嗜冷蛋白质结构研究发现，其表面的空穴(cavity)的数量与大小都高于同源的中温蛋白[50]。蛋白质表面空穴可保存大量的亲水基团，结合更多的水分子，通过加强内部溶解性从而增加酶的折叠活性[50]。比如来自菌株解脂酸发光杆菌(Photobacterium lipolyticum)的嗜冷M37脂肪酶就含有表面空穴[51]。降低蛋白质表面空穴的稳定性，可提高蛋白质螺旋的柔性，提高代谢底物向酶的结合位点移动的效率。通过比较嗜冷M37脂肪酶和来自嗜中温菌米黑根毛霉(Rhizomucor miehei)的同源脂肪酶也发现了嗜冷酶有着更宽的含氧的阴离子穴(oxy anion hole)，此类修饰可使M37脂肪酶结合更多的水分子，有助于降低酶在作用过程中需要的能量，从而降低最适生长温度[51]。
上述研究主要是针对单一蛋白质或者单个菌株进行的分析，这些规律是否适用于多菌株甚至群落水平呢？最近，Shen等[10]对Arthrobacter中由9个来自南北极和青藏高原的菌株形成的低温环境单系分支进行了整体的蛋白质稳定性分析。结果显示，寒冷环境单系类群的δ吉布斯自由能(ΔG)在温度低于0 ℃时要显著高于对照组的中温菌株。较高的δ吉布斯自由能对应较高的构象柔性和更低的热稳定性，通过蛋白质热稳定性曲线预测证实了寒冷环境特有类群的菌株通过氨基酸序列的改变增强了低温活性，但是降低了高温耐受性。这项结果表明，基于单一蛋白质或者单个菌株分析获得的结论也可能是适用于多个菌株甚至整个群落。随着人工智能技术的进步，如AlphaFold的出现，蛋白质结构组学领域正在经历一场变革。不依赖模板的高精度、高通量建模将会给环境微生物学领域带来新的发现[52]。
2.3 DNA结合蛋白维持低温下的转录和翻译冷休克反应是指突然暴露在低温环境下，微生物会上调或者下调一些基因的表达量的过程[53]。冷休克过程可以分为适应期和低温生长期，在适应期，低温诱导蛋白的表达量达到峰值，非低温诱导蛋白的表达量受到抑制; 适应期之后开始进入低温适应性生长期，这时低温诱导蛋白的表达量开始下降并逐渐趋于平稳，微生物所表达的全部蛋白质会调整到一个新的低温适应性模式[54]。对比嗜冷甲烷叶菌(Methanolobus psychrophilus)在4 ℃和18 ℃条件下基因表达特征，发现总共有1 295个基因的表达量发生了明显的改变，约占细菌全部基因的40%[55]。菌株奥奈达希瓦氏菌(Shewanella oneidensis)在8 ℃和15 ℃条件下分别有785和546个基因的表达量发生了明显的变化[56]。这种冷休克反应通常能在很短的时间内发生，如恶臭假单胞菌(Pseudomonas putida)在温度从30 ℃降低到10 ℃后，2 h内就有2 337个基因的表达量发生了改变[57]。低温下高表达的主要是编码冷休克蛋白相关的基因，冷休克蛋白主要是一类单链DNA结合蛋白，可调控一系列的细胞过程，包括转录、翻译、蛋白质折叠和细胞膜流动性[23, 58]。另外一些在低温下高表达的基因与RNA解旋酶以及核糖体的加工与成熟相关。其中，RNA解旋酶可以降低DNA和RNA二级结构的稳定性，有利于启动基因的转录。核糖体结合因子A (RbfA)的高表达有助于低温下核糖体的加工和成熟，RbfA的过度表达可以将冷休克反应后的滞后时间缩短一半，从而使微生物更快地适应低温并促进蛋白质合成[59]。研究发现，翻译起始因子IF2 (initiation factor 2)在冷休克细胞的核糖体组装和成熟中也发挥重要作用[60]。
2.4 维持低温下细胞膜的流动性低温对微生物的另一个显著影响是降低细胞膜的流动性，而细胞膜的流动性是保持细胞功能的关键因素。相应地，嗜冷菌进化出了低温下调整细胞膜流动性的能力[61-62]。这些策略包括增加多不饱和脂肪酸含量、改变脂肪酸组成类型、降低脂肪酸的极性以及反式异构向顺式异构转变[61-63]。实验发现，在较低的生长温度下，伯顿嗜甲基甲烷拟球菌(Methanococcoides burtonii)细胞中不饱和脂肪酸的比例显著提高[64]。转录组和生理实验的研究发现，低温可以引起细胞膜合成相关基因(如脂肪酸、磷脂脂肪酸、肽聚糖和糖基转移酶)的快速上调表达，在嗜冷菌深海发光杆菌(P. profundum) SS9中也发现了细胞膜合成相关基因的富集现象[65]。蛋白质组的研究发现，膜运输蛋白在低温下的表达量上调，以应对低温导致的细胞膜溶解率降低的不利因素[66-67]。如膜运输转运载体可通过加强对营养物质、相容性溶质和膜多肽的吸收从而应对低温和高渗透压的环境压力[66-68]。
色素在保持低温下细胞膜的流动性中也有重要的作用，是极地和高山地区微生物应对环境压力的重要策略之一[69]。极性和非极性的色素在许多南极和青藏高原的细菌中都能产生，色素被认为是细胞膜流动性的缓冲剂，可以帮助细胞膜在面对温度波动时保持粘性; 色素还可以通过直接吸收紫外辐射来起到保护作用，随机突变实验表明，产色素缺陷型菌株对紫外线更加敏感[29, 70-72]。
2.5 低温下的渗透压调节低温导致的细胞质中的水分形成冰晶，将直接损伤细胞并引起渗透压失衡[70]。嗜冷菌通过吸收甘氨酸、甜菜碱和蔗糖等相容性溶质降低细胞内的凝固点，同时还可以抵御脱水和高渗透压从而获得低温下保持活性的能力[58, 70]。实验发现，大肠杆菌(Escherichia coli)在低温下通过上调海藻糖合成量来抵抗低温带来的损伤，此过程对于E. coli在低温下生存十分关键[73]，进一步通过转录组实验发现，海藻糖合成基因otsA和otsB可在低温下被诱导表达[74]。一些嗜冷菌可产生抗冻蛋白或者冰结合蛋白，此类蛋白质可结合并限制冰晶的生长，起到降低细胞质冰点的作用[75]。另外，冰核蛋白可通过促进冰晶的形成从而阻止过冷水的产生[76]。
胞外多糖(exopolysaccharides，EPS)也是一种低温保护剂，嗜冷菌在低温下可以产生大量的EPS[77-81]。EPS可降低水的凝固点和冰核形成的温度，锁住水分、营养物质、离子并且提高细胞表面粘度，促进细胞聚集和生物膜的形成，还可保护胞外酶[78-80]。实验发现，添加EPS可促进冷红科尔韦尔氏菌(Colwellia psychrerythraea) 34H在-1- -20 ℃的代谢速率[82]。实验还发现，由硅藻北极直链藻(Melosira arctica)，圆柱拟脆杆藻(Fragilariopsis cylindrus)和嗜冷菌C. psychrerythraea产生的EPS可阻止脱盐过程并破坏生长中冰晶的微结构，从而避免微生物细胞在结冰的过程中受到损伤[83-85]。因此，EPS通过改变冰的渗透性，锁住冰中的盐分，通过提高盐分而阻止冰的生长，从而为低温环境中的微生物创造有利的生存环境[79-80]。
2.6 低温下的氧化损伤由于低温下氧气的溶解度增加，导致活性氧(reactive oxygen species，ROS)浓度的增加，从而使细胞在寒冷环境的胁迫下容易发生氧化损伤。ROS为含有氧的化学反应分子，包括超氧自由基(O2-)和羟自由基(HO-)等[86]。ROS可对细胞结构造成严重的损害，如造成脂质过氧化破坏细胞流动性、引起蛋白质氧化、导致DNA碱基修饰和键断裂等[87-89]。因此，防止氧化损伤对于微生物在低温下生存尤为重要。
嗜冷菌有多种克服在寒冷环境下造成的氧化损伤的策略。研究表明，编码ROS解毒的基因在冷应激下上调，如过氧化氢酶(catalase)、2种超氧化物歧化酶(SodA和SodC)，硫醇过氧化物酶(Bcp)以及硫氧还蛋白和硫氧还蛋白还原酶(TrxA和TrxB)等，这些酶具有强大的抗氧化活性，能抵抗氧化应激。超氧化物歧化酶催化超氧阴离子转化为过氧化氢，再通过过氧化氢酶和过氧化物酶催化发生歧化反应[90-91]。TrxA和TrxB在保持细胞内硫醇-二硫化物平衡的同时，也清除ROS[92]。通过对嗜盐浮游假交替单胞菌(Pseudoalteromonas haloplanktis) TAC125基因组序列的分析发现，其含有编码H2O2和超氧化物酶具有活性的基因，且该生物对H2O2具有明显抗性，在抵抗ROS损伤中发挥重要作用[93]。耐压希瓦氏菌(S. piezotolerans) WP3在低温和H2O2的胁迫下表现出良好的耐受性，基于基因组学分析，其有关编码H2O2清除的基因ccpA2和gpx分别上调了1.6倍和2.6倍[94]。除过氧化氢和超氧化歧化酶外，红球菌(Rhodococcus sp.) CNS16在低温下表现出过氧化氢酶和超氧化物歧化酶活性的丧失，并利用硫氧还蛋白依赖性的过氧化物酶来参与清除细菌中的ROS[95]。涅斯特连科氏菌(Nesterenkonia sp.) AN1与Nesterenkonia sp. PF2B19中均发现了编码与ROS解毒相关的基因，如过氧化氢酶、超氧化物歧化酶，硫醇过氧化物酶以及硫氧还蛋白和硫氧还蛋白还原酶[96-97]。亚精胺和腐胺是最常见的细胞保护多胺，通过作用于核酸和中和ROS来增强分子功能[98]。多胺氨基丙基转移酶SpeE2仅在冷胁迫下表达，冷胁迫催化丙胺基团从氨基供体S-腺苷甲硫氨酸不可逆地转移到腐胺以产生亚精胺。反之，腐胺由鸟氨酸或精氨酸分别通过鸟氨酸脱羧酶或精氨酸脱羧酶产生[99]。近期研究发现，在冷胁迫下的嗜冷菌 萨拉曼卡假单胞菌(P. helmanticensis)除了过氧化物酶和超氧化物歧化酶上调外，2-酮精氨酸脱羧酶上调了35.51倍，表明产生了保护性多胺的亚精胺和腐胺，从而来抵抗氧化应激[100]。此外，还有一些嗜冷菌可能通过缩短代谢途径，不产生或者是较少产生ROS，从源头上减少氧自由基的来源[101]。
2.7 微生物对低温环境的适应性进化Cryobacterium是一类高度适应了低温环境的放线菌，其绝大部分成员分离自南北极和青藏高原等寒冷环境。对78株Cryobacterium的最适生长温度特征和基因组进行联合比较分析发现，它们之间的最适生长温度存在梯度差异，并且与系统发育分支的聚类密切相关。有着相对较低最适生长温度的菌株其基因组更加偏好于A/U结尾的同义密码子，表现为密码子第三位的GC含量显著降低。由自然选择所导致的较低的GC含量使相应DNA具有更高的柔韧性，进而确保DNA在低温下以合适的分子动态正常行使功能。而这个自然选择压力可能主要来自冰川环境的胁迫[36]。
嗜冷菌基因组的可塑性促进了其对低温极端环境的适应性进化[102]，为了探索细菌的基因组功能、基因含量和动力学变化是否受冰川环境胁迫因素驱动，Liu等[103]对21个嗜冷性冷杆菌Cryobacterium菌株的基因组进行了比较基因组学分析，发现嗜冷低温细菌的基因组含量发生了更多的动态变化，并且它们的基因组中涉及应激反应，运动性和趋化性的基因数量显著多于嗜温性低温细菌。基于多基因串联系统发育树的birth-and-death模型分析，发现在中温菌株嗜中温冷杆菌(C. mesophilum)分化后，嗜冷Cryobacterium的最近共同祖先基因组经历了一个快速扩增的过程(通过1 168个基因获得了最多的基因)。基因组的扩增带来了关键基因，这些基因主要和辅酶、维生素和色素、碳水化合物和膜运输等功能相关。嗜冷Cryobacterium菌株的氨基酸取代率比嗜中温菌株低两个数量级。然而，在嗜冷的Cryobacterium菌株中并未发现明显更多的冷休克基因，这表明，尽管冷休克基因对于嗜冷菌是必不可少的，但多拷贝并不是微杆菌科(Microbacteriaceae)冷适应的关键因素。由冰川环境胁迫因素驱动的广泛的基因水平转移可能是嗜冷细菌抵抗冰川上的低温、寡营养和高紫外线辐射的策略。此项研究结果与泛基因组分析所发现的关键推论一致，原核生物的关键进化过程不是点突变，而是通过基因水平转移和基因丢失造成的基因替换[104]。
3 展望低温环境中的微生物类群丰富，在复杂类群中判断哪些类群在该生态系统中发挥关键作用还十分困难。很大一部分从低温环境中分离的菌株最低生长温度在4 ℃左右，这个温度显然要高于其生存环境大部分时间的温度，判断这些类群是否能在原位环境发挥生态功能是一项具有挑战性的工作[13, 105-106]。那些在实验室中没有表现出0 ℃及以下温度活性的类群，可能仅仅是因为低温被保存下来的外源中温微生物，也可能是在实验条件下无法完全模拟其原位生存条件，如物种间群体感应条件的缺失。还可能是脱离相互作用的物种和微环境之后，这些微生物无法在0 ℃及以下温度表现出显著的生长迹象[107]。但是如Arthrobacter、Cryobacterium，微小杆菌属(Exiguobacterium)、黄杆菌属(Flavobacterium)和极单胞菌属(Polaromonas)等属中能够形成低温环境(可操作)单系分支，并且在0 ℃及以下温度具有较高生长活性的类别，可以优先作为研究微生物对低温环境适应性的模式物种[10, 27, 108]。而随着基因组数据(包括来自纯培养菌株的全基因组、单细胞测序全基因组和宏基因组组装的全基因组)的持续增加，结合不同温度条件下的生长控制实验，将会有更多的低温环境单系类群被发现。这些类群的基因组和生理特征更能代表微生物对特定环境的适应性[109]。那些在基因组和生理特征上与中温菌区分开的低温环境类群，将可能在指示气候变化、节能减排和农业生产中发挥重要作用。
由于人类的活动，全球气候与环境发生着剧烈的变化。冰冻圈是气候系统最敏感的圈层，气候变暖对冰川生态系统的影响要比其他区域更为深刻和敏感[110-111]。气候变化可以直接或者间接影响微生物的群落及其功能，在冰川环境中可表现为低温特有类群竞争优势的丧失，被广布类群所替代，导致微生物群落结构改变; 在永久冻土中，参与好氧和厌氧碳分解、氨氧化以及产甲烷相关的功能基因丰度在短期变暖过程中显著增加，从而促进二氧化碳和甲烷等温室气体的排放，对气候变暖形成正反馈[10-11, 112-116]。因此，了解低温环境类群对于冰川和冻土等生态系统的气候变化的响应将有助于人们了解气候变化的趋势，但目前有关冰川的增温研究还非常少，需要积累长期的观测数据。
在工业生产中，冷适应酶因其在较低的温度下就可以发挥很高的催化活性，而在降低能耗、减少碳排放中有着广泛的应用前景[117]。研究表明，在工业洗涤领域，反应体系温度每降低10 ℃就可减少30%的用电量，即相当于每次洗涤减少0.1 kg的CO2排放[64, 118]。从喜马拉雅冰川土壤中分离出来的嗜麦芽寡养单胞菌(Stenotrophomonas maltophilia) MTCC 7528和短小芽孢杆菌(Bacillus pumilus) BO1产生的嗜冷蛋白酶将来可能会在上述领域发挥重要作用[119-121]。除了在应用于洗涤行业，冷适应酶在食品、纺织等行业中也发挥着重要的应用[122]。如在食品加工过程中使用冷适应酶可以避免高温处理步骤，有助于保留风味、提高营养价值[123]。
世界上有很大一部分可耕作土地处在高寒环境中，利用能在寒冷环境中生长的低温环境类群可能会成为促进丘陵和山地等高海拔寒冷地带农业生产力的重要方法[16, 124]。已有研究表明，某些低温环境类群具有促进植物生长(如在低温下合成植物生长激素吲哚乙酸、促进溶磷作用等)以及缓解植物的生物胁迫的特性[125]。从南极、喜马拉雅山脉和其它高海拔地区分离的假单胞菌(Pseudomonas spp.)，芽孢杆菌(Bacillus spp.)，链霉菌(Streptomyces sp.) 5和小单孢菌(Micromonospora sp.) 18在低温下能够促进植物种子的萌发与生长; 而Pseudomonas spp.、Streptomyces sp. 5和Micromonospora sp. 18还可以抑制尖孢镰孢菌(Fusarium oxysporum)和晚疫病病菌(Phytophtora infestans)等植物致病菌，从而缓解植物病害[126-130]。冷适应植物生长促进微生物可以作为在寒冷环境中有效的生物肥料和生物防治剂，这为极端寒冷环境微生物资源在农业领域的应用打开了新的大门[16]。
致谢
在文章修改过程中，新南威尔士大学的Timothy J. Williams博士提供了无私帮助和指导，在此表示衷心感谢。
| [1] | Priscu JC, Johnson L, Christner BC. Earth's icy biosphere. Washington, D.C.: ASM Press, 2004. |
| [2] | Xiang SR, Shang TC, Chen Y, Jing ZF, Yao TD. Changes in diversity and biomass of bacteria along a shallow snow pit from Kuytun 51 Glacier, Tianshan Mountains, China. Journal of Geophysical Research Atmospheres, 2009, 114(G4): G04008. |
| [3] | Jungblut AD, Lovejoy C, Vincent WF. Global distribution of cyanobacterial ecotypes in the cold biosphere. The ISME Journal, 2010, 4(2): 191-202. DOI:10.1038/ismej.2009.113 |
| [4] | An L, Chen Y, Xiang SR, Shang TC, Tian LD. Differences in community composition of bacteria in four deep ice sheets in Western China. Biogeosciences Discussions, 2010, 7(1): 1167. |
| [5] | Boetius A, Anesio AM, Deming JW, Mikucki JA, Rapp JZ. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nature Reviews Microbiology, 2015, 13(11): 677-690. DOI:10.1038/nrmicro3522 |
| [6] | Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK, Fierer N. A global atlas of the dominant bacteria found in soil. Science, 2018, 359(6373): 320-325. DOI:10.1126/science.aap9516 |
| [7] | Panikov NS, Flanagan PW, Oechel WC, Mastepanov MA, Christensen TR. Microbial activity in soils frozen to below −39 ℃. Soil Biology and Biochemistry, 2006, 38(4): 785-794. DOI:10.1016/j.soilbio.2005.07.004 |
| [8] | Shen L, Yao TD, Liu YQ, Jiao NZ, Kang SC, Xu BQ, Zhang SH, Liu XB. Downward-shifting temperature range for the growth of snow-bacteria on glaciers of the Tibetan Plateau. Geomicrobiology Journal, 2014, 31(9): 779-787. DOI:10.1080/01490451.2014.891418 |
| [9] | Scholze C, Jørgensen BB, Røy H. Psychrophilic properties of sulfate-reducing bacteria in Arctic marine sediments. Limnology and Oceanography, 2021, 66(S1): S293-S302. |
| [10] | Shen L, Liu YQ, Allen MA, Xu BQ, Wang NL, Williams TJ, Wang F, Zhou YG, Liu Q, Cavicchioli R. Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution. Microbiome, 2021, 9(1): 136. DOI:10.1186/s40168-021-01084-z |
| [11] | Cary SC, McDonald IR, Barrett JE, Cowan DA. On the rocks: the microbiology of Antarctic dry valley soils. Nature Reviews Microbiology, 2010, 8(2): 129-138. DOI:10.1038/nrmicro2281 |
| [12] | Cavicchioli R. Microbial ecology of Antarctic aquatic systems. Nature Reviews Microbiology, 2015, 13(11): 691-706. DOI:10.1038/nrmicro3549 |
| [13] | Jansson JK, Taş N. The microbial ecology of permafrost. Nature Reviews Microbiology, 2014, 12(6): 414-425. DOI:10.1038/nrmicro3262 |
| [14] | Smith HJ, Foster RA, McKnight DM, Lisle JT, Littmann S, Kuypers MMM, Foreman CM. Microbial formation of labile organic carbon in Antarctic glacial environments. Nature Geoscience, 2017, 10(5): 356-359. DOI:10.1038/ngeo2925 |
| [15] | Cauvy-Fraunié S, Dangles O. A global synthesis of biodiversity responses to glacier retreat. Nature Ecology & Evolution, 2019, 3(12): 1675-1685. |
| [16] | Yarzábal LA. Perspectives for using glacial and periglacial microorganisms for plant growth promotion at low temperatures. Applied Microbiology and Biotechnology, 2020, 104(8): 3267-3278. DOI:10.1007/s00253-020-10468-4 |
| [17] | Kasana RC, Pandey CB. Exiguobacterium: an overview of a versatile genus with potential in industry and agriculture. Critical Reviews in Biotechnology, 2018, 38(1): 141-156. DOI:10.1080/07388551.2017.1312273 |
| [18] | Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA. Diversity and association of psychrophilic bacteria in Antarctic Sea ice. Applied and Environmental Microbiology, 1997, 63(8): 3068-3078. DOI:10.1128/aem.63.8.3068-3078.1997 |
| [19] | Morita RY. Psychrophilic bacteria. Bacteriological Reviews, 1975, 39(2): 144-167. DOI:10.1128/br.39.2.144-167.1975 |
| [20] | Gounot AM. Effects of temperature on the growth of psychrophilic bacteria from glaciers. Canadian Journal of Microbiology, 1976, 22(6): 839-846. DOI:10.1139/m76-121 |
| [21] | Cavicchioli R. On the concept of a psychrophile. The ISME Journal, 2016, 10(4): 793-795. DOI:10.1038/ismej.2015.160 |
| [22] | Farrell J, Rose A. Temperature effects on microorganisms. Annual Review of Microbiology, 1967, 21: 101-120. DOI:10.1146/annurev.mi.21.100167.000533 |
| [23] | D'Amico S, Collins T, Marx JC, Feller G, Gerday C. Psychrophilic microorganisms: challenges for life. EMBO Reports, 2006, 7(4): 385-389. DOI:10.1038/sj.embor.7400662 |
| [24] | Liu YQ, Priscu JC, Yao TD, Vick-Majors TJ, Michaud AB, Sheng L. Culturable bacteria isolated from seven high-altitude ice cores on the Tibetan Plateau. Journal of Glaciology, 2019, 65(249): 29-38. DOI:10.1017/jog.2018.86 |
| [25] | Shen L, Liu Y, Xu B, Wang N, Zhao H, Liu X, Liu F. Comparative genomic analysis reveals the environmental impacts on two Arcticibacter strains including sixteen Sphingobacteriaceae species. Scientific Reports, 2017, 7: 2055. DOI:10.1038/s41598-017-02191-4 |
| [26] | Rivkina EM, Friedmann EI, McKay CP, Gilichinsky DA. Metabolic activity of permafrost bacteria below the freezing point. Applied and Environmental Microbiology, 2000, 66(8): 3230-3233. DOI:10.1128/AEM.66.8.3230-3233.2000 |
| [27] | Panikov NS, Sizova MV. Growth kinetics of microorganisms isolated from Alaskan soil and permafrost in solid media frozen down to −35 ℃. FEMS Microbiology Ecology, 2007, 59(2): 500-512. DOI:10.1111/j.1574-6941.2006.00210.x |
| [28] | Gadkari PS, McGuinness LR, Männistö MK, Kerkhof LJ, Häggblom MM. Arctic tundra soil bacterial communities active at subzero temperatures detected by stable isotope probing. FEMS Microbiology Ecology, 2019, 96(2): fiz192. |
| [29] | Rodrigues DF, Tiedje JM. Coping with our cold planet. Applied and Environmental Microbiology, 2008, 74(6): 1677-1686. DOI:10.1128/AEM.02000-07 |
| [30] | Piette F, D'Amico S, Mazzucchelli G, Danchin A, Leprince P, Feller G. Life in the cold: a proteomic study of cold-repressed proteins in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Applied and Environmental Microbiology, 2011, 77(11): 3881-3883. DOI:10.1128/AEM.02757-10 |
| [31] | Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NPA. Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiology and Molecular Biology Reviews: MMBR, 2006, 70(1): 222-252. DOI:10.1128/MMBR.70.1.222-252.2006 |
| [32] | Tehei M, Zaccai G. Adaptation to extreme environments: macromolecular dynamics in complex systems. Biochimica et Biophysica Acta: BBA - General Subjects, 2005, 1724(3): 404-410. DOI:10.1016/j.bbagen.2005.05.007 |
| [33] | Hinnebusch J, Tilly K. Linear plasmids and chromosomes in bacteria. Molecular Microbiology, 1993, 10(5): 917-922. DOI:10.1111/j.1365-2958.1993.tb00963.x |
| [34] | Galtier N, Lobry JR. Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. Journal of Molecular Evolution, 1997, 44(6): 632-636. DOI:10.1007/PL00006186 |
| [35] | Meyer MM. Revisiting the relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature. Journal of Molecular Evolution, 2021, 89(3): 165-171. DOI:10.1007/s00239-020-09974-w |
| [36] | Liu Q, Song WZ, Zhou YG, Dong XZ, Xin YH. Phenotypic divergence of thermotolerance: molecular basis and cold adaptive evolution related to intrinsic DNA flexibility of glacier-inhabiting Cryobacterium strains. Environmental Microbiology, 2020, 22(4): 1409-1420. DOI:10.1111/1462-2920.14957 |
| [37] | Wang HC, Susko E, Roger AJ. On the correlation between genomic G+C content and optimal growth temperature in prokaryotes: data quality and confounding factors. Biochemical and Biophysical Research Communications, 2006, 342(3): 681-684. DOI:10.1016/j.bbrc.2006.02.037 |
| [38] | Khachane AN, Timmis KN, Dos Santos VAPM. Uracil content of 16S rRNA of thermophilic and psychrophilic prokaryotes correlates inversely with their optimal growth temperatures. Nucleic Acids Research, 2005, 33(13): 4016-4022. DOI:10.1093/nar/gki714 |
| [39] | Sato Y, Kimura H. Temperature-dependent expression of different guanine-plus-cytosine content 16S rRNA genes in Haloarcula strains of the class Halobacteria. Antonie Van Leeuwenhoek, 2019, 112(2): 187-201. DOI:10.1007/s10482-018-1144-3 |
| [40] | Cavicchioli R. Cold-adapted archaea. Nature Reviews Microbiology, 2006, 4(5): 331-343. DOI:10.1038/nrmicro1390 |
| [41] | Saunders NFW, Thomas T, Curmi PMG, Mattick JS, Kuczek E, Slade R, Davis J, Franzmann PD, Boone D, Rusterholtz K, Feldman R, Gates C, Bench S, Sowers K, Kadner K, Aerts A, Dehal P, Detter C, Glavina T, Lucas S, Richardson P, Larimer F, Hauser L, Land M, Cavicchioli R. Mechanisms of thermal adaptation revealed from the genomes of the Antarctic archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Research, 2003, 13(7): 1580-1588. DOI:10.1101/gr.1180903 |
| [42] | Siddiqui KS, Williams TJ, Wilkins D, Yau S, Allen MA, Brown MV, Lauro FM, Cavicchioli R. Psychrophiles. Annual Review of Earth and Planetary Sciences, 2013, 41: 87-115. DOI:10.1146/annurev-earth-040610-133514 |
| [43] | Siddiqui KS, Poljak A, Guilhaus M, De Francisci D, Curmi PMG, Feller G, D'Amico S, Gerday C, Uversky VN, Cavicchioli R. Role of lysine versus arginine in enzyme cold-adaptation: modifying lysine to Homo-arginine stabilizes the cold-adapted α-amylase from Pseudoalteramonas haloplanktis. Proteins: Structure, Function, and Bioinformatics, 2006, 64(2): 486-501. DOI:10.1002/prot.20989 |
| [44] | Huston AL, Haeggström JZ, Feller G. Cold adaptation of enzymes: structural, kinetic and microcalorimetric characterizations of an aminopeptidase from the Arctic psychrophile Colwellia psychrerythraea and of human leukotriene A4 hydrolase. Biochimica et Biophysica Acta: BBA-Proteins and Proteomics, 2008, 1784(11): 1865-1872. DOI:10.1016/j.bbapap.2008.06.002 |
| [45] | Michaux C, Massant J, Kerff F, Frère JM, Docquier JD, Vandenberghe I, Samyn B, Pierrard A, Feller G, Charlier P, Van Beeumen J, Wouters J. Crystal structure of a cold-adapted class C β-lactamase. The FEBS Journal, 2008, 275(8): 1687-1697. DOI:10.1111/j.1742-4658.2008.06324.x |
| [46] | Bauvois C, Jacquamet L, Huston AL, Borel F, Feller G, Ferrer JL. Crystal structure of the cold-active aminopeptidase from Colwellia psychrerythraea, a close structural homologue of the human bifunctional leukotriene A4 hydrolase. Journal of Biological Chemistry, 2008, 283(34): 23315-23325. DOI:10.1074/jbc.M802158200 |
| [47] | Sonan GK, Receveur-Brechot V, Duez C, Aghajari N, Czjzek M, Haser R, Gerday C. The linker region plays a key role in the adaptation to cold of the cellulase from an Antarctic bacterium. The Biochemical Journal, 2007, 407(2): 293-302. DOI:10.1042/BJ20070640 |
| [48] | Aghajari N, Van Petegem F, Villeret V, Chessa JP, Gerday C, Haser R, Van Beeumen J. Crystal structures of a psychrophilic metalloprotease reveal new insights into catalysis by cold-adapted proteases. Proteins, 2003, 50(4): 636-647. DOI:10.1002/prot.10264 |
| [49] | Leiros HKS, Pey AL, Innselset M, Moe EL, Leiros I, Steen IH, Martinez A. Structure of phenylalanine hydroxylase from Colwellia psychrerythraea 34H, a monomeric cold active enzyme with local flexibility around the active site and high overall stability. Journal of Biological Chemistry, 2007, 282(30): 21973-21986. DOI:10.1074/jbc.M610174200 |
| [50] | Paredes DI, Watters K, Pitman DJ, Bystroff C, Dordick JS. Comparative void-volume analysis of psychrophilic and mesophilic enzymes: structural bioinformatics of psychrophilic enzymes reveals sources of core flexibility. BMC Structural Biology, 2011, 11: 42. DOI:10.1186/1472-6807-11-42 |
| [51] | Jung SK, Jeong DG, Lee MS, Lee JK, Kim HK, Ryu SE, Park BC, Kim JH, Kim SJ. Structural basis for the cold adaptation of psychrophilic M37 lipase from Photobacterium lipolyticum. Proteins, 2008, 71(1): 476-484. DOI:10.1002/prot.21884 |
| [52] | Cramer P. AlphaFold2 and the future of structural biology. Nature Structural & Molecular Biology, 2021, 28(9): 704-705. |
| [53] | Graumann P, Marahiel MA. Some like it cold: response of microorganisms to cold shock. Archives of Microbiology, 1996, 166(5): 293-300. DOI:10.1007/s002030050386 |
| [54] | Horn G, Hofweber R, Kremer W, Kalbitzer HR. Structure and function of bacterial cold shock proteins. Cellular and Molecular Life Sciences: CMLS, 2007, 64(12): 1457-1470. DOI:10.1007/s00018-007-6388-4 |
| [55] | Chen ZJ, Yu HY, Li LY, Hu SN, Dong XZ. The genome and transcriptome of a newly described psychrophilic archaeon, Methanolobus psychrophilus R15, reveal its cold adaptive characteristics. Environmental Microbiology Reports, 2012, 4(6): 633-641. |
| [56] | Gao HC, Wang Y, Liu XD, Yan TF, Wu LY, Alm E, Arkin A, Thompson DK, Zhou JZ. Global transcriptome analysis of the heat shock response of Shewanella oneidensis. Journal of Bacteriology, 2004, 186(22): 7796-7803. DOI:10.1128/JB.186.22.7796-7803.2004 |
| [57] | Frank S, Schmidt F, Klockgether J, Davenport CF, Gesell Salazar M, Völker U, Tümmler B. Functional genomics of the initial phase of cold adaptation of Pseudomonas putida KT2440. FEMS Microbiology Letters, 2011, 318(1): 47-54. DOI:10.1111/j.1574-6968.2011.02237.x |
| [58] | Casanueva A, Tuffin M, Cary C, Cowan DA. Molecular adaptations to psychrophily: the impact of 'omic' technologies. Trends in Microbiology, 2010, 18(8): 374-381. DOI:10.1016/j.tim.2010.05.002 |
| [59] | Dammel CS, Noller HF. Suppression of a cold-sensitive mutation in 16S rRNA by overexpression of a novel ribosome-binding factor, RbfA. Genes & Development, 1995, 9(5): 626-637. |
| [60] | Brandi A, Piersimoni L, Feto NA, Spurio R, Alix JH, Schmidt F, Gualerzi CO. Translation initiation factor IF2 contributes to ribosome assembly and maturation during cold adaptation. Nucleic Acids Research, 2019, 47(9): 4652-4662. DOI:10.1093/nar/gkz188 |
| [61] | Deming JW. Psychrophiles and polar regions. Current Opinion in Microbiology, 2002, 5(3): 301-309. DOI:10.1016/S1369-5274(02)00329-6 |
| [62] | Chintalapati S, Kiran MD, Shivaji S. Role of membrane lipid fatty acids in cold adaptation. Cellular and Molecular Biology: Noisy Le Grand, France, 2004, 50(5): 631-642. |
| [63] | Guan ZQ, Tian B, Perfumo A, Goldfine H. The polar lipids of Clostridium psychrophilum, an anaerobic psychrophile. Biochimica et Biophysica Acta: BBA-Molecular and Cell Biology of Lipids, 2013, 1831(6): 1108-1112. |
| [64] | Nichols DS, Miller MR, Davies NW, Goodchild A, Raftery M, Cavicchioli R. Cold adaptation in the Antarctic archaeon Methanococcoides burtonii involves membrane lipid unsaturation. Journal of Bacteriology, 2004, 186(24): 8508-8515. DOI:10.1128/JB.186.24.8508-8515.2004 |
| [65] | Lauro FM, Tran K, Vezzi A, Vitulo N, Valle G, Bartlett DH. Large-scale transposon mutagenesis of Photobacterium profundum SS9 reveals new genetic loci important for growth at low temperature and high pressure. Journal of Bacteriology, 2008, 190(5): 1699-1709. DOI:10.1128/JB.01176-07 |
| [66] | Cacace G, Mazzeo MF, Sorrentino A, Spada V, Malorni A, Siciliano RA. Proteomics for the elucidation of cold adaptation mechanisms in Listeria monocytogenes. Journal of Proteomics, 2010, 73(10): 2021-2030. DOI:10.1016/j.jprot.2010.06.011 |
| [67] | Bakermans C, Tollaksen SL, Giometti CS, Wilkerson C, Tiedje JM, Thomashow MF. Proteomic analysis of Psychrobacter cryohalolentis K5 during growth at subzero temperatures. Extremophiles: Life Under Extreme Conditions, 2007, 11(2): 343-354. DOI:10.1007/s00792-006-0042-1 |
| [68] | Durack J, Ross T, Bowman JP. Characterisation of the transcriptomes of genetically diverse Listeria monocytogenes exposed to hyperosmotic and low temperature conditions reveal global stress-adaptation mechanisms. PLoS One, 2013, 8(9): e73603. DOI:10.1371/journal.pone.0073603 |
| [69] | Dieser M, Greenwood M, Foreman CM. Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arctic, Antarctic, and Alpine Research, 2010, 42(4): 396-405. DOI:10.1657/1938-4246-42.4.396 |
| [70] | Chattopadhyay MK. Mechanism of bacterial adaptation to low temperature. Journal of Biosciences, 2006, 31(1): 157-165. DOI:10.1007/BF02705244 |
| [71] | Shen L, Liu YQ, Wang NL, Jiao NZ, Xu BQ, Liu XB. Variation with depth of the abundance, diversity and pigmentation of culturable bacteria in a deep ice core from the Yuzhufeng Glacier, Tibetan Plateau. Extremophiles: Life Under Extreme Conditions, 2018, 22(1): 29-38. DOI:10.1007/s00792-017-0973-8 |
| [72] | Johler S, Stephan R, Hartmann I, Kuehner KA, Lehner A. Genes involved in yellow pigmentation of Cronobacter sakazakii ES5 and influence of pigmentation on persistence and growth under environmental stress. Applied and Environmental Microbiology, 2010, 76(4): 1053-1061. DOI:10.1128/AEM.01420-09 |
| [73] | Kandror O, DeLeon A, Goldberg AL. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. PNAS, 2002, 99(15): 9727-9732. DOI:10.1073/pnas.142314099 |
| [74] | Phadtare S, Inouye M. Genome-wide transcriptional analysis of the cold shock response in wild-type and cold-sensitive, quadruple-csp-deletion strains of Escherichia coli. Journal of Bacteriology, 2004, 186(20): 7007-7014. DOI:10.1128/JB.186.20.7007-7014.2004 |
| [75] | Celik Y, Drori R, Pertaya-Braun N, Altan A, Barton T, Bar-Dolev M, Groisman A, Davies PL, Braslavsky I. Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth. PNAS, 2013, 110(4): 1309-1314. DOI:10.1073/pnas.1213603110 |
| [76] | Kawahara H. The structures and functions of ice crystal-controlling proteins from bacteria. Journal of Bioscience and Bioengineering, 2002, 94(6): 492-496. DOI:10.1016/S1389-1723(02)80185-2 |
| [77] | Feng S, Powell SM, Wilson R, Bowman JP. Extensive gene acquisition in the extremely psychrophilic bacterial species Psychroflexus torquis and the link to sea-ice ecosystem specialism. Genome Biology and Evolution, 2014, 6(1): 133-148. DOI:10.1093/gbe/evt209 |
| [78] | Nichols CAM, Guezennec J, Bowman JP. Bacterial exopolysaccharides from extreme marine environments with special consideration of the southern ocean, sea ice, and deep-sea hydrothermal vents: a review. Marine Biotechnology: New York, NY, 2005, 7(4): 253-271. DOI:10.1007/s10126-004-5118-2 |
| [79] | Qin GK, Zhu LZ, Chen XL, Wang PG, Zhang YZ. Structural characterization and ecological roles of a novel exopolysaccharide from the deep-sea psychrotolerant bacterium Pseudoalteromonas sp. SM9913. Microbiology: Reading, England, 2007, 153(Pt 5): 1566-1572. |
| [80] | De Los Ríos A, Wierzchos J, Sancho LG, Ascaso C. Exploring the physiological state of continental Antarctic endolithic microorganisms by microscopy. FEMS Microbiology Ecology, 2004, 50(3): 143-152. DOI:10.1016/j.femsec.2004.06.010 |
| [81] | Collins T, Margesin R. Psychrophilic lifestyles: mechanisms of adaptation and biotechnological tools. Applied Microbiology and Biotechnology, 2019, 103(7): 2857-2871. DOI:10.1007/s00253-019-09659-5 |
| [82] | Junge KR, Eicken H, Swanson BD, Deming JW. Bacterial incorporation of leucine into protein down to-20 degrees C with evidence for potential activity in sub-eutectic saline ice formations. Cryobiology, 2006, 52(3): 417-429. DOI:10.1016/j.cryobiol.2006.03.002 |
| [83] | Ewert M, Deming JW. Selective retention in saline ice of extracellular polysaccharides produced by the cold-adapted marine bacterium Colwellia psychrerythraea strain 34H. Annals of Glaciology, 2011, 52(57): 111-117. DOI:10.3189/172756411795931868 |
| [84] | Krembs C, Eicken H, Deming JW. Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(9): 3653-3658. DOI:10.1073/pnas.1100701108 |
| [85] | Aslam SN, Cresswell-Maynard T, Thomas DN, Underwood GJC. Production and characterization of the intra- and extracellular carbohydrates and polymeric substances (EPS) of three sea-ice diatom species, and evidence for a cryoprotective role for EPS. Journal of Phycology, 2012, 48(6): 1494-1509. DOI:10.1111/jpy.12004 |
| [86] | De Maayer P, Anderson D, Cary C, Cowan DA. Some like it cold: understanding the survival strategies of psychrophiles. EMBO Reports, 2014, 15(5): 508-517. DOI:10.1002/embr.201338170 |
| [87] | Aruoma OI, Kaur H, Halliwell B. Oxygen free radicals and human diseases. Journal of the Royal Society of Health, 1991, 111(5): 172-177. DOI:10.1177/146642409111100506 |
| [88] | Houée-Levin C, Bobrowski K. The use of the methods of radiolysis to explore the mechanisms of free radical modifications in proteins. Journal of Proteomics, 2013, 92: 51-62. DOI:10.1016/j.jprot.2013.02.014 |
| [89] | Halgand F, Houée-Lévin C, Weik M, Madern D. Remote oxidative modifications induced by oxygen free radicals modify T/R allosteric equilibrium of a hyperthermophilic lactate dehydrogenase. Journal of Structural Biology, 2020, 210(2): 107478. DOI:10.1016/j.jsb.2020.107478 |
| [90] | Ebara S, Shigemori Y. Alkali-tolerant high-activity catalase from a thermophilic bacterium and its overexpression in Escherichia coli. Protein Expression and Purification, 2008, 57(2): 255-260. DOI:10.1016/j.pep.2007.09.015 |
| [91] | Moustafa DA, Jain N, Sriranganathan N, Vemulapalli R. Identification of a single-nucleotide insertion in the promoter region affecting the sodC promoter activity in Brucella neotomae. PLoS One, 2010, 5(11): e14112. DOI:10.1371/journal.pone.0014112 |
| [92] | Ballal A, Manna AC. Control of thioredoxin reductase gene (trxB) transcription by SarA in Staphylococcus aureus. Journal of Bacteriology, 2010, 192(1): 336-345. DOI:10.1128/JB.01202-09 |
| [93] | Médigue C, Krin E, Pascal G, Barbe V, Bernsel A, Bertin PN, Cheung F, Cruveiller S, D'Amico S, Duilio A, Fang G, Feller G, Ho C, Mangenot S, Marino G, Nilsson J, Parrilli E, Rocha EPC, Rouy Z, Sekowska A, Tutino ML, Vallenet D, Von Heijne G, Danchin A. Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Research, 2005, 15(10): 1325-1335. DOI:10.1101/gr.4126905 |
| [94] | Xie Z, Jian HH, Jin Z, Xiao X. Enhancing the adaptability of the deep-sea bacterium Shewanella piezotolerans WP3 to high pressure and low temperature by experimental evolution under H2O2 stress. Applied and Environmental Microbiology, 2018, 84(5): e02342-e02317. |
| [95] | Kloska A, Cech GM, Sadowska M, Krause K, Szalewska-Pałasz A, Olszewski P. Adaptation of the marine bacterium Shewanella baltica to low temperature stress. International Journal of Molecular Sciences, 2020, 21(12): 4338. DOI:10.3390/ijms21124338 |
| [96] | Aliyu H, De Maayer P, Cowan D. The genome of the Antarctic polyextremophile Nesterenkonia sp. AN1 reveals adaptive strategies for survival under multiple stress conditions. FEMS Microbiology Ecology, 2016, 92(4): fiw032. DOI:10.1093/femsec/fiw032 |
| [97] | Singh P, Kapse N, Gowdaman V, Tsuji M, Singh SM, Dhakephalkar PK. Comparative genomic analysis of Arctic permafrost bacterium Nesterenkonia sp. PF2B19 to gain insights into its cold adaptation tactic and diverse biotechnological potential. Sustainability, 2021, 13(8): 4590. DOI:10.3390/su13084590 |
| [98] | Limsuwun K, Jones PG. Spermidine acetyltransferase is required to prevent spermidine toxicity at low temperatures in Escherichia coli. Journal of Bacteriology, 2000, 182(19): 5373-5380. DOI:10.1128/JB.182.19.5373-5380.2000 |
| [99] | Koh HY, Park H, Lee JH, Han SJ, Sohn YC, Lee SG. Proteomic and transcriptomic investigations on cold-responsive properties of the psychrophilic Antarctic bacterium Psychrobacter sp. PAMC 21119 at subzero temperatures. Environmental Microbiology, 2017, 19(2): 628-644. DOI:10.1111/1462-2920.13578 |
| [100] | Kumar S, Suyal DC, Yadav A, Shouche Y, Goel R. Psychrophilic Pseudomonas helmanticensis proteome under simulated cold stress. Cell Stress & Chaperones, 2020, 25(6): 1025-1032. |
| [101] | Tribelli PM, López NI. Reporting key features in cold-adapted bacteria. Life: Basel, Switzerland, 2018, 8(1): 8. |
| [102] | Allen MA, Lauro FM, Williams TJ, Burg D, Siddiqui KS, De Francisci D, Chong KWY, Pilak O, Chew HH, de Maere MZ, Ting L, Katrib M, Ng C, Sowers KR, Galperin MY, Anderson IJ, Ivanova N, Dalin E, Martinez M, Lapidus A, Hauser L, Land M, Thomas T, Cavicchioli R. The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation. The ISME Journal, 2009, 3(9): 1012-1035. DOI:10.1038/ismej.2009.45 |
| [103] | Liu YQ, Shen L, Zeng YH, Xing TT, Xu BQ, Wang NL. Genomic insights of Cryobacterium isolated from ice core reveal genome dynamics for adaptation in glacier. Frontiers in Microbiology, 2020, 11: 1530. DOI:10.3389/fmicb.2020.01530 |
| [104] | Koonin EV, Makarova KS, Wolf YI. Evolution of microbial genomics: conceptual shifts over a quarter century. Trends in Microbiology, 2021, 29(7): 582-592. DOI:10.1016/j.tim.2021.01.005 |
| [105] | Xiang SR, Yao TD, An LZ, Xu BL, Wang JX. 16S rRNA sequences and differences in bacteria isolated from the Muztag Ata glacier at increasing depths. Applied and Environmental Microbiology, 2005, 71(8): 4619-4627. DOI:10.1128/AEM.71.8.4619-4627.2005 |
| [106] | Zhang XF, Yao TD, Tian LD, Xu SJ, An LZ. Phylogenetic and physiological diversity of bacteria isolated from Puruogangri ice core. Microbial Ecology, 2008, 55(3): 476-488. DOI:10.1007/s00248-007-9293-3 |
| [107] | Miller MB, Bassler BL. Quorum sensing in bacteria. Annual Review of Microbiology, 2001, 55: 165-199. DOI:10.1146/annurev.micro.55.1.165 |
| [108] | Liu Q, Li W, Liu D, Li L, Li J, Lv N, Liu F, Zhu B, Zhou Y, Xin Y, Dong X. Light stimulates anoxic and oligotrophic growth of glacial Flavobacterium strains that produce zeaxanthin. The ISME Journal, 2021, 15(6): 1844-1857. DOI:10.1038/s41396-020-00891-w |
| [109] | Hutchins DA, Jansson JK, Remais JV, Rich VI, Singh BK, Trivedi P. Climate change microbiology—problems and perspectives. Nature Reviews Microbiology, 2019, 17(6): 391-396. DOI:10.1038/s41579-019-0178-5 |
| [110] |
Qin DH, Zhou BT, Xiao CD. Progress in studies of cryospheric changes and their impacts on climate of China. Acta Meteorologica Sinica, 2014, 72(5): 869-879.
(in Chinese) 秦大河, 周波涛, 效存德. 冰冻圈变化及其对中国气候的影响. 气象学报, 2014, 72(5): 869-879. |
| [111] |
Yao TD, Wu GJ, Xu BQ, Wang WC, Gao J, An BS. Asian water tower change and its impacts. Bulletin of Chinese Academy of Sciences, 2019, 34(11): 1203-1209.
(in Chinese) 姚檀栋, 邬光剑, 徐柏青, 王伟财, 高晶, 安宝晟. 亚洲水塔变化与影响. 中国科学院院刊, 2019, 34(11): 1203-1209. |
| [112] | Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, Behrenfeld MJ, Boetius A, Boyd PW, Classen AT, Crowther TW, Danovaro R, Foreman CM, Huisman J, Hutchins DA, Jansson JK, Karl DM, Koskella B, Mark Welch DB, Martiny JBH, Moran MA, Orphan VJ, Reay DS, Remais JV, Rich VI, Singh BK, Stein LY, Stewart FJ, Sullivan MB, Van Oppen MJH, Weaver SC, Webb EA, Webster NS. Scientists' warning to humanity: microorganisms and climate change. Nature Reviews Microbiology, 2019, 17(9): 569-586. DOI:10.1038/s41579-019-0222-5 |
| [113] | Xue K, Yuan MM, Shi ZJ, Qin Y, Deng Y, Cheng L, Wu L, He Z, Van Nostrand JD, Bracho R, Natali S, Schuur EAG, Luo C, Konstantinidis KT, Wang Q, Cole JR, Tiedje JM, Luo Y, Zhou J. Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming. Nature Climate Change, 2016, 6(6): 595-600. DOI:10.1038/nclimate2940 |
| [114] | Song YY, Song CC, Ren JS, Ma XY, Tan WW, Wang XW, Gao JL, Hou AX. Short-term response of the soil microbial abundances and enzyme activities to experimental warming in a boreal peatland in northeast China. Sustainability, 2019, 11(3): 590. DOI:10.3390/su11030590 |
| [115] | Song YY, Jiang L, Song CC, Wang XW, Ma XY, Zhang H, Tan WW, Gao JL, Hou AX. Microbial abundance and enzymatic activity from tussock and shrub soil in permafrost peatland after 6-year warming. Ecological Indicators, 2021, 126: 107589. DOI:10.1016/j.ecolind.2021.107589 |
| [116] | Johnston ER, Hatt JK, He ZL, Wu LY, Guo X, Luo YQ, Schuur EAG, Tiedje JM, Zhou JZ, Konstantinidis KT. Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(30): 15096-15105. DOI:10.1073/pnas.1901307116 |
| [117] | Bhatia RK, Ullah S, Hoque MZ, Ahmad I, Yang YH, Bhatt AK, Bhatia SK. Psychrophiles: a source of cold-adapted enzymes for energy efficient biotechnological industrial processes. Journal of Environmental Chemical Engineering, 2021, 9(1): 104607. DOI:10.1016/j.jece.2020.104607 |
| [118] | Nielsen PH, Skagerlind P. Cost-neutral replacement of surfactants with enzymes-a shortcut to environmental improvement for laundry washing. HPC Today, 2007, 4: 3-7. |
| [119] | Kuddus M, Ramteke PW. Cold-active extracellular alkaline protease from an alkaliphilic Stenotrophomonas maltophilia: production of enzyme and its industrial applications. Canadian Journal of Microbiology, 2009, 55(11): 1294-1301. DOI:10.1139/W09-089 |
| [120] | Farooq S, Nazir R, Ganai SA, Ganai BA. Isolation and characterization of a new cold-active protease from psychrotrophic bacteria of Western Himalayan glacial soil. Scientific Reports, 2021, 11: 12768. DOI:10.1038/s41598-021-92197-w |
| [121] | Furhan J, Nissar J. Cold-adapted serine metalloprotease from Serratia DLCP2: purification, characterization and industrial potential. Applied Biochemistry and Microbiology, 2021, 57(1): 40-47. DOI:10.1134/S0003683821010087 |
| [122] | Dhaulaniya AS, Balan BJ, Kumar M, Agrawal PK, Singh DK. Cold survival strategies for bacteria, recent advancement and potential industrial applications. Archives of Microbiology, 2019, 201(1): 1-16. DOI:10.1007/s00203-018-1602-3 |
| [123] | Siddiqui KS. Some like it hot, some like it cold: temperature dependent biotechnological applications and improvements in extremophilic enzymes. Biotechnology Advances, 2015, 33(8): 1912-1922. DOI:10.1016/j.biotechadv.2015.11.001 |
| [124] |
Wang Y, Gong CJ. Cold-adapted microorganisms and research progress of agricultural application. Biological Chemical Engineering, 2020, 6(5): 144-147.
(in Chinese) 王奕, 宫春杰. 低温微生物及其在农业生产中的应用研究进展. 生物化工, 2020, 6(5): 144-147. DOI:10.3969/j.issn.2096-0387.2020.05.041 |
| [125] | Selvakumar G, Kundu S, Joshi P, Nazim S, Gupta AD, Gupta HS. Growth promotion of wheat seedlings by Exiguobacterium acetylicum 1P (MTCC 8707) a cold tolerant bacterial strain from the Uttarakhand Himalayas. Indian Journal of Microbiology, 2010, 50(1): 50-56. DOI:10.1007/s12088-009-0024-y |
| [126] | Berríos G, Cabrera G, Gidekel M, Gutiérrez-Moraga A. Characterization of a novel Antarctic plant growth-promoting bacterial strain and its interaction with Antarctic hair grass (Deschampsia antarctica Desv). Polar Biology, 2013, 36(3): 349-362. DOI:10.1007/s00300-012-1264-6 |
| [127] | Yarzábal LA, Monserrate L, Buela L, Chica E. Antarctic Pseudomonas spp. promote wheat germination and growth at low temperatures. Polar Biology, 2018, 41(11): 2343-2354. DOI:10.1007/s00300-018-2374-6 |
| [128] | Bisht SC, Mishra PK, Joshi GK. Genetic and functional diversity among root-associated psychrotrophic Pseudomonad's isolated from the Himalayan plants. Archives of Microbiology, 2013, 195(9): 605-615. DOI:10.1007/s00203-013-0908-4 |
| [129] | Gesheva V. Production of antibiotics and enzymes by soil microorganisms from the windmill Islands region, Wilkes Land, East Antarctica. Polar Biology, 2010, 33(10): 1351-1357. DOI:10.1007/s00300-010-0824-x |
| [130] | Wu HJ, Gu Q, Xie YL, Lou ZY, Xue PQ, Fang L, Yu CJ, Jia DD, Huang GC, Zhu BC, Schneider A, Blom J, Lasch P, Borriss R, Gao XW. Cold-adapted Bacilli isolated from the Qinghai-Tibetan Plateau are able to promote plant growth in extreme environments. Environmental Microbiology, 2019, 21(9): 3505-3526. DOI:10.1111/1462-2920.14722 |