Subpopulations of hyphae secrete proteins or resist heat stress in <i>Aspergillus oryzae</i> colonies

Tegelaar, Martin; Bleichrodt, Robert-Jan; Nitsche, Benjamin; Wösten, Han A. B.

doi:10.1111/1462-2920.14863

Cited by 18 publications

(20 citation statements)

References 39 publications

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“…Although A. oryzae SSC has been widely utilized in fermentation and brewing industries, cellular and physiological studies on A. oryzae SSC have not yet been conducted well. Recently, it was revealed that transcriptional and translational heterogeneity in multicellular A. oryzae cells is related to protein secretion in stress responses [ 137 ]. Moreover, it was shown that under stress conditions, stress granules that consist of non-translating messenger ribonucleoproteins are formed around the hyphal tip region of A. oryzae cells [ 138 ], although the underlying molecular and physiological details of stress granule formation need further analyses.…”

Section: Discussionmentioning

confidence: 99%

Membrane Traffic in Aspergillus oryzae and Related Filamentous Fungi

Higuchi

2021

JoF

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The industrially important filamentous fungus Aspergillus oryzae, known as the yellow Koji mold and also designated the Japanese National fungus, has been investigated for understanding the intracellular membrane trafficking machinery due to the great ability of valuable enzyme production. The underlying molecular mechanisms of the secretory pathway delineate the main secretion route from the hyphal tip via the vesicle cluster Spitzenkörper, but also there is a growing body of evidence that septum-directed and unconventional secretion occurs in A. oryzae hyphal cells. Moreover, not only the secretory pathway but also the endocytic pathway is crucial for protein secretion, especially having a role in apical endocytic recycling. As a hallmark of multicellular filamentous fungal cells, endocytic organelles early endosome and vacuole are quite dynamic: the former exhibits constant long-range motility through the hyphal cells and the latter displays pleiomorphic structures in each hyphal region. These characteristics are thought to have physiological roles, such as supporting protein secretion and transporting nutrients. This review summarizes molecular and physiological mechanisms of membrane traffic, i.e., secretory and endocytic pathways, in A. oryzae and related filamentous fungi and describes the further potential for industrial applications.

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Section: Discussionmentioning

confidence: 99%

Membrane Traffic in Aspergillus oryzae and Related Filamentous Fungi

Higuchi

2021

JoF

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“…By plugging the pores, intercompartmental and interhyphal cytoplasmic mixing is interrupted (Bleichrodt et al 2012(Bleichrodt et al , 2015a. Intact growing hyphae of Aspergillus oryzae (Bleichrodt et al 2012), Aspergillus niger (Tegelaar et al 2019), and Zymoseptoria tritici (2017b) plug their pores with Woronin bodies, while hyphae of the basidiomycete Schizophyllum commune close their pores with the septal pore cap (van Peer et al 2010). Environmental conditions impact incidence of septal closure in S. commune (van Peer et al 2009), A. oryzae and A. niger (Tegelaar et al 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Intact growing hyphae of Aspergillus oryzae (Bleichrodt et al 2012), Aspergillus niger (Tegelaar et al 2019), and Zymoseptoria tritici (2017b) plug their pores with Woronin bodies, while hyphae of the basidiomycete Schizophyllum commune close their pores with the septal pore cap (van Peer et al 2010). Environmental conditions impact incidence of septal closure in S. commune (van Peer et al 2009), A. oryzae and A. niger (Tegelaar et al 2019). Low glucose levels reduce plugging incidence in S. commune, while presence of antibiotics, heat shock, and hypertonic shock promote septal closure (van Peer et al 2009).…”

Section: Introductionmentioning

confidence: 99%

“…Low glucose levels reduce plugging incidence in S. commune, while presence of antibiotics, heat shock, and hypertonic shock promote septal closure (van Peer et al 2009). Plugging incidence of septa of A. oryzae is affected by heat treatment, low pH conditions, C-starvation and N-starvation, while that of A. niger is affected by exposure to heat, high pH, and hypertonic conditions (Tegelaar et al 2019). Incidence of septal closure in Aspergillus also increases in time.…”

Section: Introductionmentioning

confidence: 99%

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Apical but not sub-apical hyphal compartments are self-sustaining in growth

Tegelaar

Lans

Wösten

2020

Antonie van Leeuwenhoek

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It was recently demonstrated that apical compartments of Aspergillus niger hyphae are selfsustaining in growth. This was shown by assessing the growth rate of individual hyphae before and after dissection of the second compartment. Using the same methodology, it is here demonstrated that single apical compartments of the septate fungi Penicillium chrysogenum and Schizophyllum commune as well as the 500-lm-apical region of the non-septate fungus Rhizopus stolonifer are also self-sustaining in growth. In contrast, single 2nd compartments (obtained by dissection of the first and third compartment) of the septate fungi or the region between 500 and 1000 lm from tips of R. stolonifer were severely impacted in their growth rate. In addition, it is shown that existing or newly formed branches originating from the 2nd compartments function as a backup system for hyphal growth when the apical part of the hypha of the three studied fungi is damaged. Together, it is concluded that the apical compartments/zones of the studied fungi are self-sustaining in growth. In contrast, the subapical region is not self-sustaining but functions as a backup once the apical zone is damaged. This back up system is relevant in nature because the apices of hyphae are the first to be exposed to (a)biotic stress conditions when entering an unexplored substrate.

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“…Germination of conidia initiates the colonization of the substrate resulting in an interconnected hyphal network called mycelium (Adams et al, 1998). Hyphae in the mycelium specialize by forming secretion hyphae, resistor hyphae and aerial hyphae Tegelaar et al, 2020). Both thin and wide aerial hyphae are distinguished.…”

Section: General Introductionmentioning

confidence: 99%

Interaction between the opportunistic pathogen Aspergillus fumigatus and its host

Keizer¹

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ContentsChapter 1 General Introduction 1 Chapter 2 EphA2-dependent internalization of Aspergillus fumigatus conidia in A549 lung cells is modulated by DHN-melanin 23 Chapter 3 The protective role of DHN-melanin against hydrogen peroxide revisited: no role in protection of conidia of the opportunistic human pathogen Aspergillus fumigatus 49 Chapter 4 LaeA-dependent production of small molecules of Aspergillus niger that interact with immune receptors 69 Chapter 5 Comparison of virulence and genomic differences of five Aspergillus fumigatus isolates shows that Af293 is less virulent 99 Chapter 6 Summary and General Discussion 141 157 Dankwoord Curriculum vitae List of Publications 5 Conidia and hyphal cell wallThe cell wall protects hyphae and conidia from environmental stress (Bernard & Latgé, 2001). The main structural components of the cell wall of A. fumigatus hyphae are ⍺(1,3)-glucan, β(1,3)-glucan, mannan, galactomannan and chitin, where glucans represent 50 -60 % of the cell wall, mannan and galactomannan between 20 -30 %, while the remaining 10 -20 % of the cell wall consists of chitin (Bowman & Free, 2006;Latgé et al., 2017) (Figure 2). Chitin and ⍺(1,3)-glucan form a rigid scaffold for the fungal cell wall (Kang et al., 2018). Chitin is linked via a β(1,4)-linkage to the β(1,3)-glucan matrix on top of the chitin and ⍺(1,3)-glucan scaffold (Fontaine et al., 2000; Kang et al., 2018). The outer layer of the cell wall consists of a dynamic shell of mannose and ⍺(1,3)-glucan and glycoproteins such as galactomannan and galactosaminogalactan (GAG), the latter is only found in the vegetative mycelium (Fontaine et al., 2011; Kang et al., 2018).Several enzymes are needed to produce the cell wall polysaccharides. The A. fumigatus genome contains 8 chitin synthase (CHS) genes that encode enzymes that polymerize GlcNAc into chitin (Mellado et al., 1995). Only deletion of the chsA and chsE genes reduces chitin levels in the cell wall (Aufauvre-Brown et al., 1997;Rogg et al., 2011). Yet, single deletion of each of the CHS genes causes a growth defect (Muszkieta et al., 2014). A plasma membrane bound glucan synthase complex produces β(1,3)-glucan in the cytoplasm using UDP-glucose as a substrate. The β(1,3)-glucan is deposited at the outer surface of the plasma membrane through a pore in the membrane. The catalytic subunit of this complex is encoded by FSK1 and is regulated via Rho GTPases (Beauvais et al., 1993;Beauvais et al., 2001). The long chains of β(1,3)-glucan are made by glucanosyltransferases, which elongate the β(1,3)-glucan chains by splitting the β(1,3)-glucan and then transferring the exposed reducing end to a non-reducing end of another β(1,3)-glucan (Mouyna et al., 2000). Deletion of the genes involved in β(1,3)-glucan synthesis decreases the amount of β(1,3)-glucan in the hyphal cell wall. This decrease is compensated by an increase of chitin and galactosaminogalactan, but also in a decrease in galactomannan (Dichtl et al., 2015). The ⍺(1,3)-glucan is synthesized by the ⍺(1,3)-glucan synthases (AGS1, AG...

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Subpopulations of hyphae secrete proteins or resist heat stress in Aspergillus oryzae colonies

Cited by 18 publications

References 39 publications

Membrane Traffic in Aspergillus oryzae and Related Filamentous Fungi

Membrane Traffic in Aspergillus oryzae and Related Filamentous Fungi

Apical but not sub-apical hyphal compartments are self-sustaining in growth

Interaction between the opportunistic pathogen Aspergillus fumigatus and its host

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