Elsevier

Harmful Algae

Volume 107, July 2021, 102050
Harmful Algae

Original Article
Exploration of resting cysts (stages) and their relevance for possibly HABs-causing species in China

https://doi.org/10.1016/j.hal.2021.102050Get rights and content

Highlights

  • Reviewed diversity, distribution, and implication of resting cysts of dinoflagellates and other groups and cyst-relevant molecular characterizations in China.

  • Identified 106 species of dinoflagellate resting cysts, with 64 unequivocally identified from the marine sediment.

  • K. mikimotoi, K. veneficum, A. sanguinea and A. anophagefferens proven being resting cyst (stage) producers via culture and field studies.

  • Mapped in all seas of China for the cyst distributions of A. catenella, A. pacificum, G. catenatum, K. mikimotoi, K. veneficum, A. poporum and A. anophagefferens.

  • Identified seven issues and three themes for the future research of Chinese scientists in the area.

Abstract

The studies on the species diversity, distribution, environmental implications, and molecular basis of resting cysts (stages) of dinoflagellates and a few species of other groups conducted in China during the last three decades are reviewed. The major achievements are summarized as the following five aspects: 1) The continual efforts in detecting the species diversity of resting cysts (spores) in dinoflagellates and other classes using either morphological or molecular approaches, or both, in the four seas of China, which led to identifications of 106 species of dinoflagellate resting cysts and 4 species of resting stages from other groups of microalgae, with a total of 64 species of dinoflagellate cysts and the resting stage of the brown tide-causing Aureococcus anophagefferens being unequivocally identified via molecular approaches from the sediments of Chinese coastal waters; 2) The well-known toxic and HABs-causing dinoflagellates Karenia mikimotoi, Karlodinium veneficum, Akashiwo sanguinea and the pelagophyte A. anophagefferens were proven to be resting cyst (stage) producers via laboratory studies on their life cycles and field detections of resting cysts (resting stage cells). And, via germination experiment and subsequent characterization of vegetative cells, numerous dinoflagellate species that had never been described or found to form cysts were discovered and characterized; 3) The distributions of the resting cysts of Alexandrium catenella, A. pacificum, Gymnodinium catenatum, K. mikimotoi, K. veneficum and Azadinium poporum and the resting stage cells of A. anophagefferens were morphologically and molecularly mapped in all four seas of China, with A. anophagefferens proven to have been present in the Bohai Sea for at least 1,500 years; 4) Obtaining important insights into the ‘indicator’ values of the dinoflagellate cyst assemblages in sediment cores for tracking eutrophication, environmental pollution and other anthropological influences in coastal waters; 5) Studies on the cyst-pertinent processes and genetic basis (transcriptomics together with physiological and chemical measurements) of resting cyst dormancy not only revealed the regulating patterns of some environmental factors in cyst formation and germination, but also identified many characteristically active or inactive metabolic pathways, differentially expressed genes, and the possibly vital regulating function of the phytohormone abscisic acid and a group of molecular chaperones in resting cysts. We also identified seven issues and three themes that should be addressed and explored by Chinese scientists working in the area in the future.

Introduction

Life history (or life cycle) was identified as crucial subjects in six of the 100 most fundamental questions in ecology in a review prepared by 34 ecologists and dedicated to the 100th anniversary of the British Ecological Society in 2013 (Sutherland et al., 2013). For the life history of phytoplankton, one of its most characteristic aspects is the existence of a resting stage, which has been observed and intensively investigated in dinoflagellates (the resting cyst), diatoms (resting spore), green algae (oospore or akinete), chrysophytes (stomatocyst), cyanobacteria (akinete), haptophytes, cryptophytes, raphidophytes, and euglenophytes. Regardless of the different types (e. g. produced asexually or sexually), these resting stages all are believed to play central roles in the ecology and evolution of phytoplankton (Ellegaard and Ribeiro, 2018). For instance, it has been hypothesized that the life cycle involving shifts between a haploid stage and a diploid resting stage might possibly be even a prerequisite for further eukaryote evolution (Cavalier-Smith, 2002). The resting stage of dinoflagellates is well-known as resting cysts, representing the non-motile cells that are mostly produced sexually or occasionally asexually and have a mandatory dormancy period in the sediment, which is different from the ‘temporary cyst’ produced by a morphological transformation of vegetative cell under stresses (Matsuoka and Fukuyo, 2000; Anderson et al., 2003; Bravo and Figueroa, 2014; Tang and Gobler, 2015; Tang et al., 2016). Among all abovementioned types of resting stages, resting cysts of dinoflagellates, however, have been most intensively examined from multiple facets because dinoflagellates comprise about 40% of all HABs-causing species (Jeong et al., 2021), are responsible of more than 75% of HABs events (Smayda, 1997), comprise about 50% of all protists in the surface ocean (Le Bescot et al., 2016), and possess other biologically and evolutionarily important features (Lin, 2011; Lin et al., 2015). The resting cysts are highly important in the ecology of dinoflagellates, because they are associated with 1) termination of algal blooms; 2) seeding recurrent HABs; 3) genetic recombination during sexual processes to increase the adaptation potential; 4) resistance to unfavorable environmental conditions; 5) protection from viruses, grazers, or parasite attacks; 6) provision of possible indicators for alien species invasion (Olli and Trunov, 2010; Teodora Satta et al., 2010); 7) accumulation of shellfish toxins (Dale et al., 1978); 8) preservation of “seed beds” for the group's survival in the face of catastrophic events of the Earth and environmental change (Ribeiro et al., 2011; Kremp et al., 2016); and 9) geographic expansion of populations via natural and anthropological activities (Hallegraeff and Bolch, 1991; Hallegraeff, 1993). The significance of life history and the resting cyst of dinoflagellates is also reflected in the fact, for example, that during 2005‒2008, Europe Union and the NSF of USA funded an international project (SEED Project) designed to explore the life history of HABs species and how it is regulated by environmental, physiological and genetic factors. This project led to publication of a special issue of Deep Sea Research Part II on ‘Phytoplankton life cycles and their impacts on the ecology of harmful algal blooms’ (Garcés et al., 2010). Probably the most significant consensuses obtained in the project are that 1) the transition of life cycle stages is of vital importance to the dynamics of HABs, 2) the cyst assemblage in the surface sediment represents a temporally integrated repertoire of phytoplankton species, and 3) the cyst seedbeds provide the fundamental information for the monitoring of HABs and the study on the geographic distribution and alien species invasion (Olli and Trunov, 2010; Teodora Satta et al., 2010). In addition to the significance to the ecology of dinoflagellates, resting cysts are also important in being an essential contributor of primary production and thus carbon sinker (Ellegaard and Ribeiro, 2018) and in recording and thus indicating global climate, sea level, eutrophication, and changes of other environmental factors (e. g. pH and silicate concentration) in the pre-historic and historic stages (Wall et al., 1977; Mao and Harland, 1993; Dale et al., 1999; Dale, 2001, 2009; Radi et al., 2007; Leroy et al., 2013; Liu et al., 2013). Among ~2,300 accepted species of dinoflagellates (Gómez, 2012), no more than 10% of them have been confirmed to be capable of producing resting cysts (Matsuoka and Fukuyo, 2000; Anderson et al., 2003, and other recent reports on individual species).

Due to the importance of resting cysts in the ecology of HABs caused by dinoflagellates, numerous investigations on cysts regarding this aspect have been accumulated during the past four decades (as reviewed in Anderson and Wall, 1978; Dale, 2001; Garcés et al., 2010; Bravo and Figueroa, 2014; Tang et al., 2016; Ellegaard and Ribeiro, 2018). China has a sea area of about 3 million km2 and a coastline length of 18,000 km and has observed many catastrophic HABs caused by dinoflagellates in the last decades. However, the study on resting cysts of dinoflagellates had not been initiated until the late 1980s when the National Science Foundation of China (NSFC) financially supported a Key Project on “Research on the Mechanisms of Red Tide Outbreaks along the Southeast Coast of China” led by Professor YZ Qi from Jinan University (Wang, 2007). Since 1990s, in addition to many projects awarded to individual research groups, the NSFC and the Ministry of Science and Technology of China (MoST) consecutively supported another Key Project and two of the National Basic Research Programs of China (‘973 Program’) for HABs research, which had national-wide investigators in the area involved and included surveys on resting cysts. It is noteworthy that during this early stage, our studies on dinoflagellate cysts were gratefully helped in multiple ways by the internationally prestigious scientists, e. g. Drs. DM Anderson and K Matsuoka (Qi et al., 1997; Wang et al., 2004a, b, c) together with many others from Germany, Japan, Korea, France, and USA in more recent years (e. g. U Tillmann, KN Mertens, S Ribeiro, M Ellegaard). Here, we review and synthesize our knowledge about the species diversity, distribution, and abundance (for those most important HABs-causing species) of dinoflagellate resting cysts (also including a few studies on species of other classes) in the seas of China, together with the progress in understanding other aspects of resting cysts during the past three decades.

Section snippets

The inventory of dinoflagellate resting cysts

The research on resting cysts in China started with morphological identifications of cysts from marine surface sediments using light microscopy and reference micrographs at its initial stage 1996‒2007. The studies at this stage are marked with the very first publication on living dinoflagellate cysts in China by Qi et al. (1996) and the monograph of Wang (2007), with more than a half of these works published in international and peer reviewed journals (Qi et al., 1996; Wang et al., 2001, 2004a,

Using dinoflagellate cyst record as an indicator for eutrophication and anthropological influences in coastal waters

It has been recognized by palynologists that the dinoflagellate cyst record may well convey specific information about the changes of different tempo-spatial scales in global climate and marine environment such as eutrophication and environmental pollution (e.g. Mao and Harland, 1993; Dale et al., 1999; Dale, 2001; Ribeiro et al., 2011; Leroy et al., 2013). Some particular dinoflagellate cyst species may be used as ‘indicator species’ for the environmental factors and their changes. The resting

Recent progresses in technology and trends in resting cyst-relevant studies

During recent years, in addition to works on field sediment samples, more investigations have been based on cyst germinations and clonal cultures in the laboratory for more confirmative identification and classification and for gaining more in-depth insights into the physiology and ecology of life cycle or resting cyst of dinoflagellates.

Issues identified

In retrospect of the advancements of resting cyst-relevant studies in China during the last three to four decades, we may identify a number of issues needing to be addressed. Some of them are itemized below.

  • 1)

    Regarding the exact species diversity of dinoflagellate resting cysts in the sediment of Chinese seas, we have a number of reasons to speculate that there are many more new species of dinoflagellate cysts to be detected, identified, or described (Tang et al., 2016), which necessitate

Declaration of Competing Interest

We declare no conflict of interest is associated with this manuscript, and the manuscript has been approved by all authors for publication.

Acknowledgments

We are grateful of the help of Ms. Caixia Yue, Xiaohan Liu, Fengting Li, and Xiaoying Song from the Institute of Oceanology, Chinese Academy of Sciences. This work was financially supported by the National Key R&D Program of China (No. 2017YFC1404300), the Science & Technology Basic Resources Investigation Program of China (No. 2018FY100200), the Key Deployment Project of Centre for Ocean Mega-Research of Science, Chinese Academy of Sciences (No. COMS2019Q09), and the National Science

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    1

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