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Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs
Functional Ecology ( IF 4.6 ) Pub Date : 2022-07-04 , DOI: 10.1111/1365-2435.14101
Benjamin Mueller 1, 2, 3 , Hannah J Brocke 4 , Forest L Rohwer 5 , Thorsten Dittmar 6, 7 , Jef Huisman 1 , Mark J A Vermeij 1, 2 , Jasper M de Goeij 1, 2
Affiliation  

1 INTRODUCTION

Dissolved organic matter (DOM) is a key component in the biogeochemistry and overall functioning of terrestrial, freshwater and marine ecosystems (e.g. Baines & Pace, 1991; Friedlingstein et al., 2020; Hansell & Carlson, 2001; Kalbitz et al., 2000; Thomas, 1997). Fixation of atmospheric CO2 and subsequent release of DOM by photosynthetic organisms provide a major source of organic carbon into lakes, oceans and soils (Hansell & Carlson, 2001; Thornton, 2014). Rapid consumption and modification of photosynthetically derived DOM by heterotrophic microbial communities decomposes DOM to CO2 that can be released back into the atmosphere, converts DOM into biomass (Ducklow & Carlson, 1992; Hansell et al., 2009) or sequesters it as recalcitrant DOM in the deep ocean (Hansell, 2013; Jiao et al., 2010). Shifts in the community composition of primary producers or decomposers that modify DOM production, alter DOM transformations, or affect DOM consumption may have major implications for the local, regional or even global carbon cycle.

In coastal ecosystems, the DOM pool is often primarily fuelled by abundant benthic primary producers (Ziegler & Benner, 1999; Wada & Hama, 2013; Barrón et al., 2014; Reed et al., 2015). An example is provided by tropical coral reefs, which represent some of the most productive and diverse ecosystems in the world's oceans (Hatcher, 1988; Odum & Odum, 1955). Up to 50% of the photosynthates produced on coral reefs is released as DOM into the surrounding water (Davies, 1984; Haas et al., 2011). This complex mixture of organic molecules, including polysaccharides, proteins and lipids, is not directly available to most heterotrophic organisms as food source (Carlson, 2002; Dittmar & Stubbins, 2014; Hansell & Carlson, 2001). Processing of the DOM released by corals and algae into organic particles and the subsequent transfer to higher trophic levels via the microbial loop (Azam et al., 1983) and the sponge loop (de Goeij et al., 2013) can reduce the loss of energy and nutrients stored in this locally produced DOM to the open ocean, and is therefore considered pivotal to sustain the high productivity of coral reefs under oligotrophic conditions.

A combination of anthropogenic disturbances (e.g. eutrophication, overfishing, ocean acidification, global warming) has led to a devastating decline in the abundance of scleractinian corals, and a concomitant increase in fleshy macroalgae, benthic cyanobacterial mats (BCMs) and turf algae on many reefs around the world (Gardner et al., 2003; Hoegh-Guldberg, 1999; Hughes et al., 2017; McCook et al., 2001). Since these non-calcifying taxa release more DOM per surface area than scleractinian corals (Haas et al., 2011; Mueller et al., 2014), this shift in benthic community composition results in an increase in benthic DOM production with potentially major implications for coral reef functioning (de Goeij et al., 2017; Haas et al., 2016; Pawlik et al., 2016). The relative abundance of turf algae has increased dramatically on many reefs, making them often the most abundant functional group within exposed benthic reef communities (Barott et al., 2012; Kramer, 2003; Vermeij et al., 2010). Turf algae are heterogeneous consortia of Chlorophyta, Phaeophyta and Rhodophyta commonly including filamentous cyanobacteria and a distinct community of other associated microbes (Barott et al., 2011; Connell et al., 2014; Fricke et al., 2011; Steneck & Dethier, 1994). Fast growth (Littler et al., 2006), rapid nutrient uptake (den Haan et al., 2016) and the ability to fix dinitrogen (Charpy et al., 2010; den Haan et al., 2014) allow turf algae to outcompete other reef organisms by rapidly occupying new space. Furthermore, their net areal primary production rates and dissolved organic carbon (DOC) release rates (i.e. during daylight) are among the highest reported for benthic primary producers on coral reefs (Adey & Goertemiller, 1987; Haas et al., 2010).

In general, the release of photosynthetically fixed carbon as DOC is directly linked to primary production with a positive relationship between DOC release and light availability (e.g. Baines & Pace, 1991; Cherrier et al., 2014; Zlotnik & Dubinsky, 1989). Reported DOC release rates in the dark are therefore typically much lower than DOC release rates in the light (Barrón et al., 2014; Haas et al., 2010; Mueller et al., 2014; Zlotnik & Dubinsky, 1989). In contrast, BCMs dominated by the cyanobacterium Oscillatoria bonnemaisonii not only release large quantities of DOC during the day, but also release two times more DOC at night (Brocke, Wenzhoefer, et al., 2015). Due to the absence of light, nightime DOC release is likely caused by incomplete degradation and anaerobic fermentation of carbohydrates that have accumulated in cyanobacterial cells by their photosynthetic activity during daytime, as has previously been reported for several Oscillatoria species (Heyer et al., 1989; Heyer & Krumbein, 1991; Stal & Moezelaar, 1997). Cyanobacteria typically contribute 20%–50% of the total biomass of turf algae in the Southern Caribbean and are often dominated by Oscillatoria spp. (Fricke et al., 2011). Consequently, these turf algae may also release large amounts of DOC at night (Müller, 2015), but these rates as well as their contribution to carbon cycling within reef communities have not been studied.

It is becoming increasingly evident that not only the quantity, but also the quality (i.e. bio-availability and utilization) of DOM for key DOM consumers (i.e. microbes and sponges) differs considerably among primary producers. Microbes and sponges metabolize algal-DOM faster than coral-DOM (Campana et al., 2021; Nelson et al., 2013; Rix et al., 2017; Silva et al., 2021). Algal-DOM further increases microbial respiration and fuels the fast but inefficient growth of opportunistic microbes (i.e. large amounts of DOM required to support growth; Nelson et al., 2013). This shifts the microbial community metabolism from net autotrophy to net heterotrophy (Haas et al., 2013) and depletes the local DOM pool to sustain a greater microbial biomass, instead of transferring energy and nutrients stored in DOM to higher trophic levels. This process is commonly referred to as the ‘microbialization of reefs’ (Haas et al., 2016; McDole et al., 2012).

To date, the contribution of fermentation-derived DOM released at night to the total reef-wide DOM production, its bio-availability to and utilization by microbial communities, and its potential role in the microbialization of reefs remains virtually unknown. This study therefore aims to quantify DOC released by turf algae during the day and at night (from here on referred to as ‘day-DOC’ and ‘night-DOC’) and to estimate how the contribution of this day-DOC and night-DOC release to the local DOC pool may have changed over the past 40 years on a Caribbean reef. Furthermore, we investigated the quality (i.e. C:N ratio, bio-availability and bacterial growth efficiency) of this turf-algal DOM for a natural bacterioplankton community to assess its potential contribution to the microbialization of reefs. Specifically, we (a) tested the occurrence of hypoxia at the water–turf algae interface; a prerequisite for fermentation-derived night-DOC release, (b) quantified day- and night-DOC release and net primary production by turf algae and (c) assessed the quality of these day- and night-exudates for bacterioplankton in bioassays. Lastly, we (d) extrapolated current DOC release fluxes on a coral reef site on Curaçao and (e) compared those to estimates of historic DOC release fluxes based on benthic community composition data from the 1970s at the same location.



中文翻译:

草坪藻类夜间溶解有机物释放及其在珊瑚礁微生物化中的作用

1 简介

溶解有机物(DOM)是陆地、淡水和海洋生态系统的生物地球化学和整体功能的关键组成部分(例如Baines & Pace, 1991 ; Friedlingstein et al., 2020 ; Hansell & Carlson, 2001  ; Kalbitz  et al  .2000;托马斯,  1997)。光合生物对大气中CO 2的固定以及随后释放的DOM为湖泊、海洋和土壤提供了有机碳的主要来源(Hansell & Carlson,  2001;Thornton,  2014)。异养微生物群落对光合作用产生的 DOM 进行快速消耗和修饰,将 DOM 分解为可释放回大气中的 CO 2 ,将 DOM 转化为生物质(Ducklow & Carlson, 1992;Hansell 等人,  2009)或将其作为顽固 DOM 隔离在深海中(Hansell,  2013;Jiao et al.,  2010)。改变 DOM 生产、改变 DOM 转化或影响 DOM 消耗的初级生产者或分解者群落组成的变化可能对当地、区域甚至全球碳循环产生重大影响。

在沿海生态系统中,DOM 池通常主要由丰富的底栖初级生产者提供燃料(Ziegler & Benner,  1999;Wada & Hama,  2013;Barrón 等,  2014;Reed 等,  2015)。热带珊瑚礁就是一个例子,它代表了世界海洋中最具生产力和多样性的生态系统(Hatcher,  1988;Odum & Odum,  1955)。珊瑚礁产生的光合产物中有高达 50% 以 DOM 形式释放到周围的水中(Davies,  1984;Haas 等,  2011)。这种复杂的有机分子混合物,包括多糖、蛋白质和脂质,不能直接作为大多数异养生物的食物来源(Carlson,2002;  Dittmar & Stubbins,  2014;Hansell & Carlson,  2001)。将珊瑚和藻类释放的 DOM 加工成有机颗粒,然后通过微生物循环(Azam 等, 1983)和海绵循环(de Goeij 等,  2013)转移到更高的营养级, 可以减少当地生产的 DOM 中储存的能量和营养物质输送到公海,因此被认为对于在贫营养条件下维持珊瑚礁的高生产力至关重要。

人为干扰(例如富营养化、过度捕捞、海洋酸化、全球变暖)的综合作用导致石珊瑚数量的毁灭性下降,许多珊瑚礁上的肉质大型藻类、底栖蓝藻垫(BCM)和草皮藻也随之增加。世界各地(Gardner 等人,  2003 年;Hoegh-Guldberg,  1999 年;Hughes 等人,  2017 年;McCook 等人,  2001 年)。由于这些非钙化类群单位表面积释放的 DOM 量比石珊瑚珊瑚多(Haas 等人,  2011 年;Mueller 等人,  2014 年),因此底栖群落组成的这种变化导致底栖 DOM 产量增加,这可能对生态系统产生重大影响。珊瑚礁功能(de Goeij 等人,  2017 年;Haas 等人,  2016 年;Pawlik 等人,  2016 年)。许多珊瑚礁上草皮藻类的相对丰度急剧增加,使它们通常成为暴露的底栖珊瑚礁群落中最丰富的功能群(Barott 等,2012;  Kramer,  2003;Vermeij 等,  2010)。草坪藻类是绿藻门、褐藻门和红藻门的异质群落,通常包括丝状蓝藻和其他相关微生物的独特群落(Barott 等,2011;  Connell等,  2014;Fricke 等,  2011;Steneck 和 Dethier,  1994 ) )。快速生长(Littler 等人,  2006)、快速养分吸收(den Haan 等人,2016)以及固定二氮的能力(Charpy 等人,  2010;den Haan 等人,  2014)使草坪藻类在竞争中脱颖而出其他珊瑚礁生物迅速占据新的空间。此外,它们的净面积初级生产力和溶解有机碳(DOC)释放率(即白天)是珊瑚礁底栖初级生产者中报道最高的(Adey & Goertemiller,1987;Haas 等  2010 

一般来说,光合固定碳以 DOC 的形式释放与初级生产直接相关,DOC 释放与光利用率之间呈正相关(例如 Baines & Pace,1991;Cherrier 等,2014;Zlotnik  & Dubinsky  1989  。因此,报告的黑暗中 DOC 释放率通常远低于光照中的 DOC 释放率(Barrón 等人,  2014 年;Haas 等人,  2010 年;Mueller 等人,  2014 年;Zlotnik 和 Dubinsky,  1989 年)。相比之下,以蓝藻Oscillatoria bonnemaisonii为主的 BCM不仅在白天释放大量 DOC,而且在夜间释放两倍多的 DOC (Brocke, Wenzhoefer, et al., 2015  )由于缺乏光照,夜间 DOC 的释放可能是由于白天的光合活动在蓝藻细胞中积累的碳水化合物的不完全降解和厌氧发酵造成的,正如之前对几种颤藻物种的报道(Heyer 等,1989  ;Heyer 和 Krumbein,  1991;Stal 和 Moezelaar,  1997)。蓝藻通常占南加勒比海草皮藻类总生物量的 20%–50%,并且通常以颤藻属 ( Oscillatoria spp) 为主。(弗里克等人,  2011)。因此,这些草皮藻类也可能在夜间释放大量 DOC(Müller,  2015),但这些速率及其对珊瑚礁群落内碳循环的贡献尚未得到研究。

越来越明显的是,对于主要 DOM 消费者(即微生物和海绵)来说,DOM 的数量和质量(即生物利用度和利用率)在初级生产者之间都存在很大差异。微生物和海绵代谢藻类 DOM 的速度比珊瑚 DOM 更快(Campana 等人,  2021;Nelson 等人,  2013;Rix 等人,  2017;Silva 等人,  2021)。Algal-DOM 进一步增加微生物呼吸,促进机会微生物快速但低效的生长(即需要大量 DOM 来支持生长;Nelson 等人,2013  。这将微生物群落代谢从净自养转变为净异养(Haas 等人,  2013),并耗尽局部 DOM 库以维持更大的微生物生物量,而不是将 DOM 中存储的能量和营养物质转移到更高的营养水平。这个过程通常被称为“珊瑚礁微生物化”(Haas 等人,  2016 年;McDole 等人,  2012 年)。

迄今为止,夜间释放的发酵源 DOM 对整个珊瑚礁 DOM 生产的贡献、微生物群落的生物利用度和利用以及其在珊瑚礁微生物化中的潜在作用仍然几乎未知。因此,本研究旨在量化草坪藻类在白天和夜间释放的 DOC(以下称为“白天 DOC”和“夜间 DOC”),并估计白天 DOC 和夜间的贡献如何。过去 40 年来,加勒比珊瑚礁向当地 DOC 池的 DOC 释放可能发生了变化。此外,我们还研究了天然浮游细菌群落的草皮-藻类 DOM 的质量(即 C:N 比、生物利用率和细菌生长效率),以评估其对珊瑚礁微生物化的潜在贡献。具体来说,我们(a)测试了水-草皮藻类界面缺氧的发生情况;发酵衍生的夜间 DOC 释放的先决条件,(b) 量化草坪藻类的白天和夜间 DOC 释放和净初级生产,(c) 在生物测定中评估浮游细菌这些白天和夜间分泌物的质量。最后,我们 (d) 推断了库拉索岛珊瑚礁地点当前的 DOC 释放通量,并 (e) 将其与基于同一地点 1970 年代底栖群落组成数据的历史 DOC 释放通量估计值进行了比较。

更新日期:2022-07-04
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