Insights into the loss factors of phytoplankton blooms: The role of cell mortality in the decline of two inshore Alexandrium blooms

Abstract

24While considerable effort has been devoted to understanding the factors regulating the 25 development of phytoplankton blooms, the mechanisms leading to bloom decline and 26 termination have received less attention. Grazing and sedimentation have been invoked as 27 the main routes for the loss of phytoplankton biomass, and more recently, viral lysis, 28 parasitism and programmed cell death (PCD) have been recognized as additional removal 29 factors. Despite the importance of bloom declines to phytoplankton dynamics, the 30 incidence and significance of various loss factors in regulating phytoplankton populations 31have not been widely characterized in natural blooms. To understand mechanisms 32 controlling bloom decline, we studied two independent, inshore blooms of Alexandrium 33 fundyense, paying special attention to cell mortality as a loss pathway. We observed 34 increases in the number of dead cells with PCD features after the peak of both blooms, 35 demonstrating a role for cell mortality in their terminations. In both blooms, sexual cyst 36 formation appears to have been the dominant process leading to bloom termination, as 37 both blooms were dominated by small-sized gamete cells near their peaks. Cell death and 38 parasitism became more significant as sources of cell loss several days after the onset of 39 bloom decline. Our findings show two distinct phases of bloom decline, characterized by 40 sexual fusion as the initial dominant cell removal processes followed by elimination of 41 remaining cells by cell death and parasitism. factors (Cloern 1996). Blooms occur when growth processes are dominant over losses, 47 then decline when loss processes intensify relative to growth. The mechanisms 48 underlying loss processes are diverse and poorly constrained. Traditionally, grazing by 49 heterotrophic zooplankton and sinking into the deep ocean have been considered the main 50 loss factors for phytoplankton (Calbet and Landry 2004). However, natural populations 51 and laboratory cultures often collapse abruptly due to massive cell lysis events, indicating 52 that different processes must be contributing to phytoplankton mortality (Berges and 53 Falkowski 1998;Vardi et al. 1999; Berges and Choi 2014). Virus-induced cell lysis is 54 increasingly recognized as an important alternative loss factor, with a large number of 55 viruses found in aquatic ecosystems (Brussaard 2004). There is evidence that chronic 56 parasitic infections can be an important cause of phytoplankton population crashes as 57 well (Chambouvet et al. 2008). 58Another loss mechanism that has received increased attention in recent years is 59 autocatalyzed cell mortality, such as programmed cell death (PCD). PCD is different 60 from other pathways of cell death because it is an active process that is initiated by the 61 cell itself and tightly controlled by gene expression and protein synthesis inside of the 62 cells (Bidle and Falkowski 2004). Accumulating evidence suggests that PCD occurs in 63 phytoplankton under diverse envi...

Bloom termination of the toxic dinoflagellate Alexandrium catenella: Vertical migration behavior, sediment infiltration, and benthic cyst yield

“…Bloom progression was also monitored through weekly vessel‐based surveys that began in early March and included water sampling from the observatory raft at four depths: 1 m, 3 m, 5 m, and 7 m below the surface. Abundance of A. catenella from these samples was estimated by epifluorescence microscopy after staining with an A. catenella specific ribosomal probe (Anderson et al ; Choi et al ). Subsamples from the same Niskin collections were analyzed for ammonium, nitrite + nitrate, and phosphate concentrations.…”

Characterizing phytoplankton communities in the absence of resource-based competition

“…The fact is that phytoplankton do die in nature from processes other than being eaten. For example, stress can lead to programmed cell death (Bidle 2016), viral lysis can behave in a manner that is not density-dependent (Knowles et al 2020), and other forms of disease and life cycle transitions can result in phytoplankton loss (Brussaard & Riegman 1998, Choi et al 2017). However, without a mechanistic understanding on how to predict when, where, and to what extent these mortality processes occur, it is difficult to accurately represent them in models (Taniguchi et al 2014).…”

Dinophyceae use exudates as weapons against the parasiteAmoebophryasp. (Syndiniales)

“…Parasites are important contributors to phytoplankton mortality and can even sometimes induce the demise of microalgal blooms (Brussaard, 2004; Chambouvet et al ., 2008; Vardi et al ., 2009). Amongst marine parasites, the Syndiniales Amoebophryidae (also called marine Alveolate group II, or MALVII) is a widely distributed family (Guillou et al ., 2008; de Vargas et al ., 2015), ubiquitous in marine waters, including ultra-oligotrophic ones (Siano et al ., 2011), and has been associated with the demise of toxic species (Park et al ., 2002; Chambouvet et al ., 2008; Velo-Suárez et al ., 2013; Li et al ., 2014; Choi et al ., 2017) in enriched coastal environments. Its life cycle is characterized by a free-swimming stage (zoospores, also named dinospores) followed by two successive intracellular stages (trophont then sporont) that eventually kills the host and release hundreds of dinospores.…”