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Current Biology
Dispatches
Microbial Ecology: Functional ‘Modules’ Drive
Assembly of Polysaccharide-Degrading Marine
Microbial Communities
Stephen R. Lindemann1,2,*
1
Whistler Center for Carbohydrate Research, Department of Food Science, Purdue University, West Lafayette, IN, USA
2
Department of Nutrition Science, Purdue University, West Lafayette, IN, USA
*Correspondence: lindemann@purdue.edu
https://doi.org/10.1016/j.cub.2019.03.056
Although ecological principles governing the competition of microbes for simple substrates are well-
understood, less is known about how complex, structured substrates influence ecological outcomes in
microbial communities. A new study sheds light on how marine microbial communities assemble on
polysaccharide particles modeling marine snow.
Understanding ecological responses of the ecology of microbial communities organisms compete and cooperate,
microbial communities to the complex, than does the consumption of a simple dividing metabolic labor as they degrade
structured substrates common in the substrate like glucose. Sugar monomers complexsubstrateslikepolysaccharides.
natural environment remains a central and oligomers are available to any Workreported in this issue of Current
challenge of microbial ecology. The organism in the community that can Biology sheds light on the dynamics of
mathematical relationship between transport and degrade them, as their polysaccharide-degrading marine
resourceavailability and microbial growth small size allows them to fit through microbial communities, revealing that
on simple sugars like glucose has been transporter proteins into the cell. In their assembly and dynamics depend not
knownfor over half a century [1]. contrast, however, larger oligomers and on species but on the functional
Furthermore, the ecology of microbial polymers are too large to be easily ‘modules’ they possess [10] (Figure 1).
competition for these simple substrates transported by most microbes, and Incubating particles composedof the
(that is, those that can be directly typically require hydrolysis outside the polysaccharidescommonlyproducedby
transported into the cell and metabolized) cell to produce breakdown products that marinephototrophs(agarose,chitin,
bymultiple microbesiswell known[2].As can be transported. Therefore, in the alginate, and carrageenan) embeddedin
predicted by the competitive exclusion context of a more complex substrate, the magnetichydrogelsinsurfaceseawater,
principle in ecology (also known as external degradation of substrates by the authors demonstrated that the initial
Gause’s Law [3]), any advantage of one microbes that possess the required assemblyofparticle-attached microbial
speciesingrowthonasubstratewill,over degradative enzymes has the capacity to communitieswasdominatedby
time, lead to dominance of the better produce ‘public goods’ (simpler sugars polysaccharide-specific primary
competitor; in contrast, the inferior one and other metabolic by-products) that degraders. However,thesecommunities
will either go extinct or avoid competition cross-feed other organisms lacking the reproducibly gave waytodominancebya
(for example,byadoptinganewniche)[4]. ability to hydrolyze the complex similar set of secondary degraders across
Fierce competition for simple sugars substrate, thereby stabilizing diverse all of the polysaccharides tested. These
typically keeps their environmental ecologicalinteractions[7].Recentstudies successionsrevealedabimodal
concentrations low [5]. However, the suggest that microbial communities are association between the specificity of an
ecology of microbial communities that indeed adapted for increased alternative sequence variant (ASV, a
degrade much more environmentally cooperativity in degradation of computationalproxyforasetofmicrobial
abundant polysaccharides — those that polysaccharides. For example, some genotypesidenticalacrossthesequenced
aretoolargetobetransportedintothecell assemblagesofmarineisolates exhibited regionofthe16SribosomalRNAgene)for
and require secreted degradative synergistic growth on the the polysaccharide embeddedinthe
enzymestobreakthemintotransportable polysaccharides cellulose and xylan but particle; organisms were either highly
monomersandoligomers —remains not when grown on glucose [8]. specificforoneofthefourpolysaccharides
poorly understood. The ecology of Additionally, these same communities (specialists) or highly unspecific, being
polysaccharide consumption is central to displayed less inhibition of other species successful on all of them (generalists).
the functioning of many important whengrowingonpolysaccharides when The authors recapitulated the ecology
microbial systems, impacting processes comparedwithgrowthonglucose[9].The of these interactions using isolates from
as large as global carbon flux [5] and as ability to predict microbial community the incubations, showing that prior
personal as human and animal health [6]. assembly and dynamics is a key cultivation of a specialist Psychromonas
Consumption of a complex challengeinmicrobialecologyandhinges isolate supported the growth of five
polysaccharide has different effects upon uponourunderstanding of how generalist microbes otherwise unable to
R330 CurrentBiology 29, R317–R339, May 6, 2019 ª 2019 Elsevier Ltd.
Current Biology
Dispatches
growonalginate.Genomicanalysisofthis
specialist revealed extensive enzymatic
machinery to hydrolyze and utilize
alginate; in contrast, generalist microbes
either possessedonlytheabilitytoimport
and consume smaller polysaccharide- n
derived oligosaccharides or lacked even o
this ability. Metabolomic analysis of the ssi
specialist-derived spent medium, before Succe
and after cultivation of generalists,
revealed consumption of the metabolic
byproducts of specialist growth, such as
amino acids, nucleotides, and
tricarboxylic acid cycle intermediates.
Interestingly, leakage and utilization of Metabolic
these metabolic products by primary products
degraders supports the hypothesis that Polysaccharides Oligo- and monosaccharides
they also support generalist populations
independently of their production of
lower-molecular-weight oligosaccharides
and monosaccharides as public goods
[11]. Metabolic cross-feeding of non- Primary degrader Secondary colonizers
polysaccharide-degrading microbes by Current Biology
degraders is important in maintaining
diversity in other marine systems [12] as Figure 1. Functional modularity in polysaccharide degradation governs microbial
succession on marine polysaccharide particles.
well as in host-associated [13,14] and Polysaccharide structures (blue and green chains) govern the initial recruitment of specific primary
engineered [15] microbial ecosystems. degrader organisms possessing the functional modules required for their consumption. Polysaccharide
Tofurther test the hypothesis that hydrolysis likely releases oligosaccharides and monosaccharides, as well as metabolic products of the
assemblyonpolysaccharideparticleswas primary degrader organism. These hydrolysis and metabolic products sustain largely shared groups of
secondary consumers, resulting in similarity across polysaccharides late in succession. When mixed,
baseduponfunctionalgroupsratherthan the stoichiometry of polysaccharides controls the early assembly of polysaccharide degraders, but
individual species, the authors results in similar dynamics later in succession.
investigated the assembly of mixed
polysaccharide particles (agarose– wasspecifictothepopulationscapturedin cycling ‘teams’ in the lit regions of marine
alginate and agarose–carrageenan) the sampledescribedhereorwhetherit ecosystems,togetherfunctioningas
incubated in the same seawater used for holdsgenerallytrue across multiple keystonespeciesthatsupportdiverse
the single-polysaccharide experiments. seawatersamples. generalist populations.
Usingtherelative abundancesofASVsas In a sense, the one job of the primary These data also suggest the possibility
inputs, the authors constructed a set of degradersinmarineecosystemsisto that polysaccharides, due likely to the
linear models to predict their abundances liberate and convert detrital, phototroph- tight correspondence between
onmixed-polysaccharideparticles.These derived carbon entrappedin carbohydratestructureandthespecificity
computationalmodelsdisplayedgood polysaccharidesforuse bysecondary of enzymes for carbohydrate linkages
agreementwiththeexperimentalresults, consumerorganisms.Oncethejobis [17], provide a certain number of
consistent with the hypothesis that predominantlyfinished,andadiverse independent niches that primary
communityassemblyanddynamicson particle-associated community degraders can fill, based upon which
thesepolysaccharideparticles depends established, primary degraders flee the functional modules their genomes
moreonfunctionalrolethanspecies particleinsearchofanotherone,repeating encode. This would suggest that the idea
identity. Essentially, so long as the the process [16]. The present study adds of the functional module may be better
appropriate primary degrader module for to this that the assemblage of primary considered at even higher levels of
the polysaccharide is present, succession degradersonsuchparticlesisinitially structural resolution than consumption of
continuesalongsimilartrajectories for all polysaccharide-specific, but thereafter a certain type of polysaccharide, such as
polysaccharides,presumablybecause successiondynamicsarelargelygeneral. at the level of specific carbohydrate
similar nutrients are available. Further, it Asthevastmajority(bymass)of linkages(orotherstructuralmotifswithina
suggeststhepossibilitythatassemblyand phototroph-derivednutrients areboundin polysaccharide). The polysaccharides
successionmaybepredictableforany biological polymers [5], this suggests the studied in this report are relatively simple
givenpolysaccharide structure and an notionthat primary phototrophs — along in structure (largely linear polymers with
initial pool of species.Thisobservationwill with the specific degraders of the most oneortwodifferentglycosylresiduesand
require further experimentation with abundantpolysaccharidesproducedby oneortwotypesoflinkagesamongthose
diverseassemblagesofmarinemicrobiota thesephototrophs—shouldperhaps residues) and divorced from their native
to determine whether the observed result together be considered coupled carbon- physical forms, so relatively fewer genes
Current Biology 29, R317–R339, May 6, 2019 R331
Current Biology
Dispatches
mayberequiredfortheir hydrolysis in the 4. Xu, C., and Yuan, S. (2016). Competition in polysaccharide uptake mechanism of marine
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¨
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Virology: Poxins Soothe the STING
1 1,*
Alexiane Decout and Andrea Ablasser
1
Global Health Institute, Ecole Polytechnique Federale de Lausanne, 1015 Lausanne, Switzerland
*Correspondence: andrea.ablasser@epfl.ch
https://doi.org/10.1016/j.cub.2019.03.031
Themammaliancyclicdinucleotide2’,3’-cGAMPisapotentinducerofinnateimmuneresponsesproduced
upon detection of cytosolic DNA by cGAS. The mechanisms underlying the control of intracellular cGAMP
levels remained unclear. In a new study, Eaglesham et al. identified poxins as 2’,3’-cGAMP-specific
nucleases allowing immune evasion by viruses.
cGAS(cyclic GMP-AMP synthase) and as 2’,3’-cGAMP) [1]. This molecule is to avoid excessive inflammation upon
STING(Stimulatorofinterferongene)form detected by STING, which then encountering self-DNA. Cytosolic
a major immune signaling axis allowing translocates from the endoplasmic DNAses,suchasTREX1,thatconstantly
the detection of cytosolic DNA, a critical reticulum to the Golgi apparatus to degradeDNAleakingfromthenucleus[3]
danger signal. Upon viral infection or activate a downstream signaling serveasimportantsafeguards.cGASitself
cellular damage, cGAS binds to cytosolic cascade, ultimately leading to the is an interferon-stimulated gene, and is
dsDNAandsynthesizes a second productionofantiviral type I interferon [2]. only upregulated when neededtoprotect
messenger—cyclic dinucleotide Activation of the cGAS–STINGpathway thehostcell[4].Likewise,STINGactivation
2’,3’-cyclic GMP AMP (also referred to istightlyregulatedatseverallevelsinorder requires several post-translational
R332 CurrentBiology 29, R317–R339, May 6, 2019 ª 2019 Elsevier Ltd.
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